bioRxiv preprint doi: https://doi.org/10.1101/033845; this version posted January 18, 2016.

The copyright holder for this preprint (which

was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.

Extreme positive allometry of animal adhesive pads and the size limits
of adhesion-based climbing
David Labonte∗1 , Christofer J. Clemente2 , Alex Dittrich3 , Chi-Yun Kuo4 , Alfred J. Crosby5 ,
Duncan J. Irschick6 & Walter Federle7
1,7
Department of Zoology, University of Cambridge, Cambridge, United Kingdom
2
School of Science and Engineering, The University of the Sunshine Coast, Australia
3
Department of Life Sciences, Anglia Ruskin University, Cambridget, United Kingdom
4,6
Biology Department, University of Massachusetts Amherst, USA
5
Department of Polymer Science and Engineering, University of Massachusetts Amherst, USA

Organismal functions are size-dependent whenever body surfaces supply body volumes. Larger organisms can develop
strongly folded internal surfaces for enhanced diffusion, but in many cases areas cannot be folded so that their enlargement
is constrained by anatomy, presenting a problem for larger animals. Here, we study the allometry of adhesive pad area in
225 climbing animal species, covering more than seven orders of magnitude in weight. Across all taxa, adhesive pad area
showed extreme positive allometry and scaled with weight, implying a 200-fold increase of relative pad area from mites to
geckos. However, allometric scaling coefficients for pad area systematically decreased with taxonomic level, and were close
to isometry when evolutionary history was accounted for, indicating that the substantial anatomical changes required to
achieve increases in relative pad area are limited by phylogenetic constraints. Using a comparative phylogenetic approach,
we found that the departure from isometry is almost exclusively caused by large differences in size-corrected pad area
between arthropods and vertebrates. To mitigate the expected decrease of weight-specific adhesion within closely related
taxa where pad area scaled close to isometry, data for several taxa suggest that the pads’ adhesive strength increased for
larger animals. The combination of adjustments in relative pad area for distantly related taxa and changes in adhesive
strength for closely related groups helps explain how climbing with adhesive pads has evolved in animals varying over
seven orders of magnitude in body weight. Our results illustrate the size limits of adhesion-based climbing, with profound
implications for large-scale bio-inspired adhesives.

The evolution of adaptive traits is driven by selective be used repeatedly without any loss of performance, and
pressures, but can be bound by phylogenetic, developmen- function on rough, dirty and flooded surfaces [12]. This
tal and physical constraints [1]. Integrating evolution and performance has inspired a considerable amount of work
biomechanics provides a powerful tool to unravel this com- on technical adhesives that mimic these properties [13].
plex interaction, as physical constraints can often be pre- A key challenge for both biological and bio-inspired ad-
dicted easily from first principles [2]. The influence of hesive systems is to achieve size-independent performance
physical constraints is especially evident in comparative [14, 15, 16], i. e. the maximum sustainable adhesion force,
studies across organisms which differ substantially in size F , should be proportional to the mass to be supported,
[3, 4, 5, 6]. For example, Fick’s laws of diffusion state that m. For vertically climbing animals, F is the product of the
diffusive transport becomes increasingly insufficient over maximum adhesive stress, σ, and the adhesive pad area,
large distances, explaining the development of enlarged A, each of which may change with mass (A ∝ ma and
surfaces for gas and nutrient exchange (e. g. leaves, roots, σ ∝ mb ), so that constant size-specific attachment perfor-
lungs, gills, guts) and integrated long-distance fluid trans- mance requires:
port systems (e. g. xylem/phloem, circulatory systems) in
larger animals and plants. How these systems change with m ∝ Aσ ∝ ma mb → a + b ≈ 1 (1)
size is determined by physical constraints [7, 8, 9]. While
‘fractal’ surface enlargements are possible without disrupt- where a and b are the scaling coefficients for σ and A
ing other body functions, strong positive allometry can in relation to body mass, respectively. If animals main-
conflict with anatomical constraints. For example, struc- tain geometric similarity when increasing in size, A would
tural stability demands that animals should increase the scale as m2/3 , so that the adhesion per body weight for
cross-sectional area of their bones in proportion to their large geckos (m ≈100 g) is expected to be approximately
body weight, but excessively thick leg bones can compro- 107/3 ≈200 times smaller than for tiny mites (m ≈10 µg) if
mise other physiological functions and hamper locomotion the pads’ adhesive strength σ remained unchanged (b = 0).
[3, 10, 11]. Large animals can only circumvent this problem by (i) de-
Adhesive pads are another example of an adaptive trait veloping disproportionally large adhesive pads (a > 2/3),
subject to size-dependent physical constraints. These sys- and/or (ii) systematically increasing the maximum force
tems allow animals to climb smooth vertical or inverted per unit pad area (b > 0). How do large climbing animals
surfaces, thereby opening up new habitats. Adhesive pads achieve adhesive forces equivalent to their body weight?
have evolved multiple times independently within arthro- Using the simple biomechanics argument outlined above
pods, reptiles, amphibians and mammals, and show im- as a framework, we here provide a comparative analysis
pressive performance: they are rapidly controllable, can of the allometry of adhesive pad area across 225 species,

1
 bioRxiv preprint doi: https://doi.org/10.1101/033845; this version posted January 18, 2016. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.

Insecta Reptilia Amphibia Arachnida Mammalia

9
10
RMA regression
8 pRMA regression Anura
10

107
Total pad area (µm )
2

106
Araneae
5
10

104

103
Hemiptera

102

10−5 10−4 10−3 10−2 10−1 100 101 102

Body weight (gram)
Figure 1: Allometry of pad area for 225 species, ranging from ≈ 20 µg to ≈ 200 g in body weight. Across all taxa, pad area was
directly proportional to body weight (reduced major axis regression, RMA, dashed line). The increase in the fraction
(black circles) of the total available surface area (grey circles) required to accommodate this disproportionate change is
schematically illustrated along the bottom axis, assuming that a climbing animal of 80 kg has a total body surface area
of 2m2 , comparable to a human of 80 kg and 180 cm, and that body surface area is approximately isometric. Strikingly,
scaling relationships were significantly less steep within closely related groups (representative solid lines from RMA
regressions), and closer to isometry when phylogenetic relationships were accounted for (phylogenetic RMA regression,
dotted line).

covering more than seven orders of magnitude in weight – a phylogenetic reduced major axis regression (pRMA) al-
almost the entire weight range of animals climbing with ad- lowed us to further investigate at what taxonomic level
hesive pads — and including representatives from all major major shifts in relative pad area occurred, separating the
groups of adhesion-based climbers. effects of size and ancestry. Relative pad area differed
strongly between vertebrates and arthropods, but compar-
atively little variation existed within these groups (fig. 3 A).
Results and Discussion More than 58% of the variation in residual pad area was
explained by differences between vertebrates and arthro-
Scaling of adhesive pad area pods (nested ANOVA, F1,173 =845, p<0.001, see tab. 2), so
Across all taxa, adhesive pad area showed extreme positive that body weight and phylum alone accounted for more
allometry and scaled as A ∝ m1.02 (reduced major axis re- than 90% of the total variation in pad area. Rather than
gression (RMA); see fig. 1 and tab. 1 for detailed statistics), being driven solely by variation in body size, differences in
an increase sufficient to compensate for the predicted loss relative pad area appear to be tied to characteristic fea-
of weight-specific adhesion, even if adhesive strength re- tures of the corresponding phyla, such as, for example, the
mained unchanged. Thus, adhesive pads occupy a larger presence or absence of multiple distal pads (toes) per leg
fraction of the body surface area in larger animals. Within (fig. 3 B,C). However, we also found evidence for differences
closely related taxonomic groups, however, pad area grew in relative pad area within lower taxonomic ranks. For ex-
more slowly with body mass, indicating a strong phyloge- ample, members of the gecko genus Sphaerodactylus had
netic signal (see fig. 1 and 2). considerably smaller pads than other Gekkotan lizards,
When evolutionary relationships were accounted for, the whereas Gekko lizards had particularly well-developed
observed scaling coefficient decreased dramatically, and pads (based on their relative pad area, fig.3 A). In insects,
was consistent with isometry (fig. 1, 2 and tab. 1). This hemimetabolous orders had smaller relative pad areas than
systematic change of allometric coefficients with taxonomic holometabolous orders (see fig.3 A). Adhesive pads can al-
rank suggests that phylogenetic inertia impedes a dis- low access to arboreal habitats [20, 21, 22], but they may
proportionate increase of pad area within closely related come at the cost of reduced locomotor performance in
groups (fig. 2 and 3 A). Our results thus add to a body of situations where no adhesion is required [23, 24]. Thus,
evidence suggesting that the evolutionary flexibility of allo- the multiple independent losses, gains, and reductions of
metric slopes is low and larger changes in particular traits adhesive pads in amphibians, insects, lizards and spiders
are mainly achieved by shifts of the allometric elevation [25, 26, 27, 28] likely reflect the ecological, behavioural and
[18, 19]. taxonomic diversity within these groups [29, 30].
Removal of the influence of body size by analysing the
residuals (termed ’relative pad area’ in the following) of

2
 bioRxiv preprint doi: https://doi.org/10.1101/033845; this version posted January 18, 2016. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.

Table 1: Results for generalised least squares and reduced major axis regressions describing the relationship between
log10 (adhesive pad area) (in µm2 ) and log10 (mass) (in g) across all taxa. Covariance in pad area and body mass
between related species was either ignored (uncorrected) or accounted for (corrected). Pagel’s lambda is a statistic mea-
suring the strength of phylogenetic signal (λ=1 indicates that the trait evolves like Brownian motion along the phylogeny,
whereas λ=0 indicates that the trait is not correlated with phylogeny [17].). Numbers in brackets give approximate 95%
confidence intervals of the estimated parameters where available.
Uncorrected Elevation Slope Pagel’s λ
Reduced major axis
Pad area against mass 6.91 (6.84, 6.98) 1.02 (0.97, 1.07) 0 (fixed)
Mass against pad area -6.76 (-7.08, -6.44) 0.98 (0.93, 1.03) 0 (fixed)
Generalised least squares
Pad area against mass 6.88 (6.80, 6.94) 0.95 (0.9, 1) 0 (fixed)
Mass against pad area -6.29 (-6.61, -5.96) 0.91 (0.86, 0.95) 0 (fixed)
Corrected Elevation Slope Pagel’s λ
Reduced major axis
Pad area against mass 6.54 (6.47, 6.62) 0.78 (0.74, 0.83) 0.93 (fitted)
Mass against pad area -8.38 (-8.77, -7.99) 1.28 (1.21, 1.36) 0.93 (fitted)
Generalised least squares
Pad area against mass 6.44 (6.28, 6.61) 0.70 (0.66, 0.75) 0.90 (fitted)
Mass against pad area -7.54 (-7.97, -7.10) 1.13 (1.06, 1.20) 0.83 (fitted)

The size-limits of adhesion-based climbing ted against body weight for 17 frog species from 4 families
and 12 genera [35, 36, 37, 38]. All adhesion measurements
Strong positive allometry of non-convoluted body struc-
were conducted using a tilting platform, and are thus com-
tures in organisms ranging in size over many orders of mag-
parable across studies. Over two orders of magnitude in
nitude is difficult to achieve, owing to simple anatomical
body weight, adhesion force per unit area increased with
constraints. For example, bone mass in terrestrial animals
m0.3 (RMA slope 0.3, 95% confidence interval (CI): (0.2,
is predicted to increase with mass4/3 to maintain constant
0.43), generalised least-squares (GLS) slope 0.19, 95% CI:
bone stress levels, but this would require unrealistic rela-
(0.08, 0.31)), sufficient to achieve body size-independent
tive bone masses for larger mammals (scaling up an 8-gram
adhesive performance despite an approximately isometric
shrew with ca 4% bone mass would produce a rather unfor-
growth of pad area (RMA slope 0.74, 95% CI: (0.62, 0.87),
tunate 8-tonne elephant with 400% bone mass). The actual
GLS slope 0.70, 95% CI: (0.58, 0.83)). In contrast to our
scaling coefficient is inevitably smaller (≈ 1.1) [10, 31], and
results for the allometry of pad area, this relationship re-
alternative strategies have evolved to limit bone stresses
mained virtually unchanged when phylogenetic relation-
[11].
ships were accounted for, indicating that pad performance
Maintaining a pad area proportional to body weight in
directly responded to selective pressures unconstrained by
animals ranging from 10−5 to 102 grams requires extraor-
phylogenetic history (phylogenetic RMA slope 0.28, 95%
dinary morphological changes: assuming otherwise isomet-
CI: (0.2, 0.42), phylogenetic GLS slope 0.17, 95% CI: (0.07,
ric animals, the proportion of the total body surface area
0.27), see fig. 4). Together, our results provide strong ev-
specialised as adhesive pad needs to increase by a factor of
idence that two different strategies have evolved to deal
107/3 ≈ 200. This extreme shape change may impose a size
with the physical challenges of a larger body size. These
limit for adhesion-based climbing. Scaling up the relative
strategies have been adopted at different taxonomic levels,
pad area of arthropods and small vertebrates to a human of
highlighting how phylogenetic and physical constraints can
180 cm body length and 80 kg body mass would result in an
influence the evolution of adaptive traits. Across distantly
adhesive pad area of ≈ 106.91 ·800001.02 ≈ 0.81 m2 , approxi-
related groups, leg morphology is sufficiently different to
mately 2/5 of the total available body surface area (≈ 2 m2 ,
accommodate large differences in relative pad area. Within
[33]). The required morphological changes, if at all possi-
closely related groups, where anatomical constraints result
ble, would thus be enormous, and difficult to achieve over
in a scaling of pad area closer to isometry, some taxa ap-
short evolutionary timescales. Our results therefore indi-
pear to have increased their pads’ adhesive efficiency with
cate that phylogenetic inertia restricts the ‘design space’
size. The mechanisms underlying this increase in adhesive
for evolution at least for closely related taxa. Larger ani-
strength are still unclear, but may be of considerable in-
mals within closely related taxa must therefore either cope
terest for the development of large-scale bio-inspired adhe-
with a size-related decrease in their relative attachment
sives. Various hypotheses have been proposed [14, 16, 37].
ability, or develop alternative strategies to compensate for
but still remain to be tested.
it. Recent studies on tree frogs and ants revealed that pad
adhesive strength can vary systematically with size, result-
ing in an almost body size-independent attachment abili- Force scaling and the evolution of ‘hairy’
ties despite a near-isometric growth of pad area [16, 34]. adhesive pads
Here, we extend these studies to investigate whether such
adaptations are also present above species or genus level. Arzt et al (2003) suggested that large animals with hairy
Figure 4 shows whole-body adhesion per pad area plot- adhesive pads have evolved higher hair densities to increase

3
 bioRxiv preprint doi: https://doi.org/10.1101/033845; this version posted January 18, 2016. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.

1.4 fied [87, 88, 89], and their live weight was recorded (ME5,
Insecta Amphibia
Reptilia Arachnida resolution 1 µg, max 5 g or 1202 MP, resolution 0.01 g, max
1.2 300 g, both Sartorius AG, Goettingen, Germany). Attach-
ment pads were photographed either with a Canon EOS
Estimated RMA slope

mass proportionality (Canon, Tokyo, Japan) mounted on a stereo microscope

1.0
(MZ16, Leica Microsystems Ltd., Heidelberg, Germany),
or by using scanning electron microscopy (SEM) for large
0.8 and small specimens, respectively. Some pads were imaged
whilst in contact with glass, visualised using the stereo-
isometric growth
0.6 microscope with coaxial illumination. For SEM imaging,
individual legs were dried, mounted on stubs, sputter-
0.4 coated at 65 mA for 10-20 s (K575X turbo-pump sputter,
Quorum Technologies, Sussex, UK) and examined with a
field emission gun SEM at a beam voltage of 5 kV (Leo
Kingdom Class Order Family Genus Species Gemini 1530VP, Carl-Zeiss NTS GmbH, Oberkochen, Ger-
Taxonomic rank many).

Figure 2: Change in pad allometry with taxonomic rank. For Data on toepad-bearing gecko species were collected
example, the slope of the regression line for Araneae in from live animals kept in the D.J.I. laboratory (under
fig. 1 is one data point for the rank ‘order’. Allomet- an Institutional Animal Care and Use (IACUC) proto-
ric coefficients decreased systematically, from mass- col 2012–0064 from the University of Massachusetts at
proportionality across all animals to isometry within Amherst to DJ Irschick), and preserved specimens from
genera and species. Data for the species-level allome- the American Museum of Natural History and the Museum
try are from [16, 32].
of Comparative Zoology at Harvard University. For each
specimen, photos of one fore foot were obtained by press-
their pads’ adhesive strength, an idea derived from the ing it tightly against the glass plate of an Epson Perfec-
assumption that adhesive forces scale with the width of tion V500 Photo Scanner (Seiko Epson Corp., Owa, Suwa,
individual hair tips [39]. Assuming isometric growth of Nagano, Japan) next to a ruler and taking a digital scan.
the total pad area, Arzt et al. predicted that hair density The total toepad area across all digits was measured using
would need to increase with m2/3 in order to achieve con- ImageJ v1.49r [90]. We also measured snout-vent-length
stant mass-specific adhesion, in agreement with the data (SVL, ±1 mm) from each individual using a clear plastic
presented (but see ref. [40] which showed that adhesive hair ruler. Where possible, we measured multiple conspecific
density increased with body mass only when species were individuals, and used the mean as the species value.
treated as independent data points, but not when phy- Literature data were taken from the papers’ text
logeny was considered). However, our data show that total or tables, or were extracted from figures using Web-
pad area is directly proportional to body mass across dis- PlotDigitizer 3.3 (WPD, developed by Ankit Ro-
tantly related taxa, so that a constant hair density would hatgi (http://arohatgi.info/WebPlotDigitizer), or Im-
suffice. In addition, there is no experimental evidence that ageJ v1.49m. We tested the performance of WPD with
the adhesive strength of animal adhesive pads increases an x-y plot of 20 random numbers between 1 and 1000 (x)
with decreasing size of individual contacts [16, 41]. Thus, and 0.01 and 10 000 (y) on a log-log scale, and found an
it appears unlikely that ‘force scaling’ has played an im- accuracy of ≈0.6% for the raw data.
portant role in the evolution of fibrillar adhesive systems
[42]. We used live body weights where available, and interpo-
Adhesive pads constitute a prime model system for lated live weight from body length where necessary, using
studying the link between morphology, performance and established scaling relationships [40]. A list of the included
fitness [43]. Further mechanistic and comparative studies species can be found in the appendix.
are needed to elucidate the factors driving the evolution
of these structures, and may ultimately allow us to mimic
their properties with synthetic adhesives.
Table 2: Results for a nested ANOVA on the residuals of a phy-
logenetic reduced major axis regression. η 2 is the vari-
Materials and Methods ance in residual pad area accounted for the by the
different taxonomic levels, and most of the variation
Data collection occurs between phyla.

Data were either collected by the authors or extracted from Tax. level df Mean squares F p-value η2
references [16, 29, 35, 36, 37, 38, 41, 44, 45, 46, 47, 48, 49, Phylum 1 40.25 845.16 < 0.001 0.58
50, 51, 52, 53, 54, 55, 56, 57, 58, 59, 60, 61, 62, 63, 64, 65, Class 3 0.41 8.55 < 0.001 0.02
66, 67, 68, 69, 70, 71, 72, 73, 74, 75, 76, 77, 78, 79, 80, 81, Order 12 1.02 21.43 < 0.001 0.18
82, 83, 84, 85, 86]. Family 35 0.22 4.52 < 0.001 0.11
Arthropod specimens were collected around Cambridge Residuals 173 0.05
(UK), Brisbane (Australia), or obtained from the Cam-
bridge Phasmid Study Group. All arthropods were identi-

4
 bioRxiv preprint doi: https://doi.org/10.1101/033845; this version posted January 18, 2016. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.

A
Heteroptera
todea Form
a B la t icid
ae
d e
ato Co
a sm c cin
Ph ell
id
ae

Ch
e

ry
i da

so
ltic

me
Sa

lida
ae

e
id
Cten

Syrph
eid a
Diplodactylidae
Hylidae

ct ylu s
roda
Sci

hae
nc
i da

Sp
e

Da

ct

o
ylo

kk
ida e
G
e
ra
hy
Ge
Lygo p us
d a ct yl u s Rhoptro
Small Large
Body size corrected
pad area
B

Figure 3: (A) Overview of the diversity of taxa examined in this study. Branch lengths do not reflect time or base pair substitutions
(see methods). Branches are coloured according to a maximum likelihood estimate of the ancestral state of relative pad
area (i. e. the residuals from a log-log regression of pad area against body weight), visualising systematic differences in
relative pad area between arthropods and vertebrates. All values apart from tip states are only approximate and are
not used to support any conclusions (see methods). (B & C) Cartoons depicting footpad morphology for representative
groups within the phylogeny shown above with smooth and hairy adhesive pads. Projected pad area is highlighted in
orange for each representative (see methods).

5
 bioRxiv preprint doi: https://doi.org/10.1101/033845; this version posted January 18, 2016. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.

Adhesive pad area RMA regression

2
pRMA regression

Adhesive force per pad area in kPa

Animals attach to smooth surfaces by employing spe-
cialised attachment pads on their legs. These pads are
either covered with dense arrays of fibrils (‘hairy pads’),
or are macroscopically unstructured (‘smooth pads’). In
order to compare pad areas across different taxa and pad
morphologies, the following assumptions were made: 1

1. ‘Projected’ pad area is the most meaningful measure

of contact area in comparative studies. Projected pad
area is the surface area of the foot specialised specif-
ically for generating adhesion and friction [91]. In a
fibrillar pad, inevitably only a fraction of this area 0.5
comes into surface contact, i. e. the ‘real’ contact
area is significantly smaller than the projected con-
1 10
tact area.
Body weight in gram
2. All animals employ a similar fraction of their available Figure 4: Adhesive force per area in 17 tree frog species in-
pad area when maximum performance is required. It creased with body mass, indicating that larger species
is unclear what fraction of the available pad area is possess more efficient pads. In contrast to the allom-
employed by animals of different size [16, 92, 93], and etry of pad area, this result was not significantly in-
systematic studies are lacking. However, the small fluenced by phylogeny.
number of direct contact area observations available
strongly suggest that animals often use the entire area
of their adhesive pads [91, 94], i. e. that they are not can depend on the ecological niche occupied by the an-
‘overbuilt’. We thus assume that all climbing pads imals [20, 22, 29, 59, 104]. Variation can also occur be-
are designed so that their whole area can be used in tween sexes [70, 105, 106], different legs or toes [20, 84],
critical situations. or even between populations of the same species occu-
pying different habitats [24]. For this study, we assume
3. Adhesive performance is dominated by distal pads. In- that because of the large number of samples and the
sects can have several attachment pads per leg. There wide range of body sizes included, any bias introduced
is strong evidence that these pad types differ in their by these factors can be ignored.
morphology, as well as in their performance and func-
tion during locomotion [16, 44, 65, 70, 91]. Many in- 5. Adhesive performance of ‘wet’ and ‘dry’ pads is com-
sects do not employ their distal pads when no adhe- parable. Dynamic adhesive pads are frequently cate-
sion is required [44, 65, 95, 96, 97, 98], whereas dur- gorised as ‘wet’ or ‘dry’. However, there is no evidence
ing inverted climbing, only distal pads are in surface for a functional difference between these two pad types
contact [83]. Accordingly, insects with ablated dis- [107], and indeed maximal adhesive stresses are com-
tal pads cannot cling upside down to smooth surfaces parable [16].
[44, 98]. Distal pads thus appear to be true ‘adhesive
pads’ [83]. Proximal pads, in contrast, can be ‘non- As some of the data used in this study originate from
sticky’, and may be designed as non-adhesive friction different groups, we quantified the consistency of pad area
pads [99, 100]. The distal pads are usually part of measurements among researchers. A selection of SEM im-
the pretarsus, but some insects lack a pre-tarsal pad. ages (three hairy, and seven smooth pads) were given to
In these insects, the distal tarsal pad can show simi- 10 scientists who independently measured nominal pad
lar morphological specialisations [101, 102]. Proximal area. We found an average coefficient of variation of
pads are mainly found in arthropods, but they may 17 ± 9%, which was independent of the animals’ body
also be present in frogs [35, 103]. As the contribu- weight (ANOVA, F1,8 =0.067, p=0.8). Scaling relation-
tion of proximal pads to adhesion is unclear and likely ships calculated with this dataset did not vary significantly
variable, we exclude them for this study. In most in- across scientists (slope: likelihood ratio statistic= 0.38; el-
sects, the total proximal pad area is between 3-5 times evation: Wald statistic=1.21, both df=9 and p>0.9).
larger than the distal pad area, and pad area is still
positively allometric even when proximal pads are in- Phlyogenetic and statistical analyses
cluded (reduced major axis regression slope between
0.8-0.9). In order to account for the non-independence of data from
related species, we first formed groups within which ad-
4. The variation of pad area/adhesive strength between hesive pads are likely homologous, based on their po-
different legs/toes and sexes of the same species, and sition on the leg and their structure (i. e. hairy vs.
the variation introduced by the animals’ ecology is in- smooth). These groups are (1) Squamata, (2) Anura,
dependent and randomly distributed with respect to (3) Araneae, (4) mites with smooth pads, (5) mites with
body weight. Several studies have shown that the size, hairy pads, (6) insects with tarsal hair fields (e. g. some
morphology and performance of attachment devices Coleoptera and Raphidioptera), (6) insects with smooth

6
 bioRxiv preprint doi: https://doi.org/10.1101/033845; this version posted January 18, 2016. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.

pulvilli (e. g. some Hemiptera), (7) insects with hairy pul- shared ancestors among lower taxonomic ranks possessed
villi (e. g. some Diptera), (8) insects with unfoldable arolia adhesive pads. Ancestral state estimates are solely used
(some Hymenoptera), (8) insects with non-eversible arolia to visualise systematic differences at the tip-level, and no
(e. g. some Polyneoptera, Hemiptera and Lepidoptera), conclusions are based on them.
(9) insects with specialised distal euplantula (some Poly-
neoptera), (10) insects with tibial pads (e. g. some aphids). Scaling of pad performance in tree frogs
These groups were all connected directly to the root of
the tree, so that analogous structures share no branch, All data are from whole-animal force measurements, con-
and thus the respective elements in the error covariance ducted using a tilting platform. In total, we extracted data
matrix of our linear models are zero [108]. Within this for pad area and body weight for 17 species belonging to 4
groups, we assembled a tree topology from phylogenies families from references [35, 36, 37, 38]. The phylogenetic
published for the constituent groups (Anura [109], Squa- tree underlying the phylogenetic regressions was extracted
mata [110], Aranae [28], Insecta [111], Blattodea [112], from the detailed phylogeny in [109], and is shown in fig. S2
Coleoptera [113], Diptera [114], Hemiptera [115, 116], Hy- in the Supplementary Information.
menoptera [117, 118]. As statistically supported branch
lengths were not available, comparative phylogenetic pro-
Acknowledgements:We are sincerely grateful to all our
cedures which allow for more complex evolutionary mod-
colleagues who readily shared published and unpublished data
els, such as Ornstein-Uhlenbeck models [119, 120], were with us: Aaron M. Bauer, Jon Barnes, Niall Crawford, Thomas
not feasible. Instead, we performed phylogenetic gener- Endlein, Hanns Hagen Goetzke, Thomas E. Macrini, Anthony
alised least squares on 10.000 trees with randomised branch P. Russell & Joanna M. Smith. This study was supported by
lengths that were rendered ultrametric via a correlated rate research grants from the UK Biotechnology and Biological Sci-
model [121]. In order to account for the uncertainty of ences Research Council (BB/I008667/1) to WF, the Human
the phylogenetic error covariance structure, Pagel’s λ was Frontier Science Programme (RGP0034/2012) to DI, AJC and
estimated simultaneously via a maximum likelihood opti- WF, the Denman Baynes Senior Research Fellowship to DL and
misation [17, 122]. The fitted coefficients were normally a Discovery Early Career Research Fellowship (DE120101503)
distributed, with a coefficient of variation below 1% (see to CJC.
fig. S1 in Supplementary Information). For simplicity, we
report results for an ultrametric tree calculated from a tree Appendix
with all branch lengths set to 1.
All analyses involving pad area and weight were per- The following species were included:
formed on log10 -transformed values, and with the the rou-
tines implemented in the R packages nlme v.3.1-118, ape Amphibia: Anura, Dendrobatidae: Mannophryne trini-
v.3.1-1, and phytools v.0.3-93 in R v.3.1.3 [123, 124]. There tatis (Garman, 1887), Hemiphractidae: Flectonotus fitzgeraldi
is some controversy as to whether (reduced) major axis or (Parker, 1933), Hylidae: Dendropsophus microcephalus (Cope,
1886); Dendropsophus minusculus (Rivero, 1971); Dendrop-
ordinary least squares regression is more appropriate for es-
sophus minutus (Peters, 1872); Hyla cinerea (Schneider,
timating allometric coefficients from data containing both 1799); Hyla versicolor LeConte, 1825; Hypsiboas boans (Lin-
‘measurement’ and ‘biological’ error [18, 19, 125, 126, 127]. naeus, 1758); Hypsiboas crepitans (Wied-Neuwied, 1824);
We thus report results for both techniques, and note that Hypsiboas geographicus (Spix, 1824); Hypsiboas punctatus
the key results of this study hold independent of what re- (Schneider, 1799); Litoria caerulea (White, 1790); Osteopilus
gression model is applied. septentrionalis (Duméril & Bibron, 1841); Phyllodytes au-
An alternative method to account for relatedness is to ratus (Boulenger, 1917); Phyllomedusa trinitatis Mertens,
monitor the change of the estimated parameters as one 1926; Scinax ruber (Laurenti, 1768); Smilisca phaeota (Cope,
moves up in taxonomic rank. We performed multiple re- 1862); Sphaenorhynchus lacteus (Daudin, 1801); Trachy-
duced major axis regressions across all taxa, and separately cephalus venulosus (Laurenti, 1768), Craugastoridae: Pristi-
mantis euphronides (Schwartz, 1967), Ranidae: Staurois gut-
within the taxonomic levels class, order, family and genus
tatus (Günther, 1858), Rhacophoridae: Rhacophorus pardalis
(for example, all Hymenoptera provide one allometric slope Gühnter, 1858
data point within the level ‘order’). Within the taxonomic
levels, groups were only included if the weight range of the Arachnida: Araneae, Ctenidae: Ctenus curvipes (Key-
available species exceeded a factor of 3, and if data for at serling, 1881); Ctenus sinuatipes Pickard-Cambridge, 1897;
least 4 different groups from the next sub-level were avail- Ctenus sp. 3 Walckenaer, 1805; Cupiennius coccineus
able (e. g. an order was included if at least four families Pickard-Cambridge, 1901; Cupiennius getazi Simon, 1891;
were represented). Cupiennius salei (Keyserling, 1877); Phoneutria boliviensis
In order to visualise the effect of evolutionary history (Pickard-Cambridge, 1897), Philodromidae: Philodromus au-
on body size-corrected pad area, residuals from a phy- reolus (Clerck, 1757); Philodromus dispar Walckenaer, 1826,
logenetic reduced major axis regression were used to es- Salticidae: Evarcha arcuata (Clerck, 1757); Marpissa mus-
cosa (Clerck, 1757); Salticus scenicus (Clerck, 1757); Sitti-
timate maximum likelihood ancestral states for all nodes
cus pubescens (Fabricius, 1775); Pseudeuophrys lanigera (Si-
and along the branches via the method described in [128]. mon, 1871), Theraphosidae: Aphonopelma seemanni (Pickard-
These values are only rough estimates, first because we do Cambridge, 1897), Thomisidae: Misumenops spec.
not have statistically supported branch lengths, second be- Mesostigmata, Laelapidae: Androlaelaps schaeferi (Till,
cause the species sampling in our phylogeny is incomplete, 1969)
third because we do not account for the influence of relative Trombidiformes, Tetranychidae: Tetranychus cinnabarinus
pad area on diversification rate, and fourth, because only Boudreaux, 1956; Tetranychus urticae (Koch, 1836)

7
 bioRxiv preprint doi: https://doi.org/10.1101/033845; this version posted January 18, 2016. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.

Insecta: Blattodea, Blaberidae: Gromphadorhina porten- cius, 1781)

tosa (Schaum, 1853); Nauphoeta cinerea (Olivier, 1789), Blat-
tellidae: Blattella germanica Linnaeus, 1767, Blattidae: Blatta
Mammalia: Chiroptera, Myzopodidae: Myzopoda aurita
orientalis Linnaeus, 1758; Periplaneta americana (Linnaeus,
Milne-Edwards & A. Grandidier, 1878
1758); Periplaneta australasiae Fabricius, 1775; Supella supel-
lectilium (Serville, 1839)
Coleoptera, Brentidae: Cylas puncticollis (Boheman, 1833), Reptilia: Squamata, Dactyloidae: Anolis auratus Daudin,
Cantharidae: Cantharis rustica Fallén, 1807; Rhagonycha 1802; Anolis biporcatus Wiegmann, 1834; Anolis capito (Pe-
fulva Scopoli, 1763, Cerambycidae: Agrianome Spinicollis ters, 1863); Anolis carolinensis Voigt, 1832; Anolis cristatellus
(Macleay, 1827); Clytus arietis (Linnaeus, 1758), Chrysomel- (Duméril & Bibron, 1837); Anolis cupreus (Hallowell, 1860);
idae: Altica lythri Aubé, 1843; Cassida canaliculata Laichart- Anolis distichus (Cope, 1861); Anolis equestris (Merrem, 1820);
ing, 1781; Chrysolina americana (Linnaeus, 1758); Chrysolina Anolis evermanni (Stejneger, 1904); Anolis frenatus (Cope,
fastuosa Scopoli, 1763; Chrysolina menthastri (Suffrian, 1851); 1899); Anolis garmani (Stejneger, 1899); Anolis grahami (Gray,
Chrysolina polita (Linnaeus, 1758); Clytra quadripunctata Lin- 1845); Anolis humilis (Peters, 1863); Anolis leachi (Duméril
naeus, 1758; Cryptocephalus spec. Geoffroy, 1762; Galerucella & Bibron, 1837); Anolis lemurinus (Cope, 1861); Anolis lim-
nymphaeaei (Linnaeus, 1758); Gastrophysa viridula (De Geer, ifrons (Cope, 1871); Anolis lineatopus Gray, 1840; Anolis li-
1775); Hemisphaerota cyanea (Say, 1824); Leptinotarsa decem- onotus (Cope, 1861); Anolis pentaprion (Cope, 1863); Anolis
lineata Say, 1824; Oulema melanopus (Linnaeus, 1758); Psyl- poecilopus (Cope, 1862); Anolis polylepis (Peters, 1874); Ano-
liodes chrysocephalus (Linnaeus, 1758), Cleridae: Trichodes lis pulchellus Duméril & Bibron, 1837; Anolis sagrei (Duméril
alvearius (Fabricius, 1792), Coccinellidae: Adalia bipunctata & Bibron, 1837); Anolis valencienni (Duméril & Bibron,
(Linnaeus, 1758); Coccinella septempunctata (Linnaeus, 1758); 1837), Diplodactylidae: Correlophus ciliatus Guichenot, 1866,
Harmonia axyridis (Pallas, 1773); Henosepilachna vigintioctop- Gekkonidae: Chondrodactylus bibronii (Smith, 1846); Gehyra
unctata (Fabricius, 1775); Psyllobora vigintiduopunctata (Lin- mutilata (Wiegmann, 1834); Gehyra oceanica (Lesson 1830);
naeus, 1758); Subcoccinella vigintiquatuorpunctata (Linnaeus, Gehyra vorax Girard, 1858; Gekko athymus Brown & Alcala,
1758), Pyrochroidae: Pyrochroa coccinea Linnaeus, 1762, Sil- 1962; Gekko gecko (Linnaeus, 1758); Gekko gigante Brown &
phidae: Nicrophorus spec. Fabricius, 1775 Alcala, 1978; Gekko japonicus (Schlegel, 1836); Gekko min-
Dermaptera, Forficulidae: Forficula auricularia Linnaeus, dorensis Taylor, 1919; Gekko monarchus (Taylor, 1917); Gekko
1758 palawanensis Taylor, 1925; Gekko romblon (Brown & Alcala,
Diptera, Calliphoridae: Calliphora vicina Robineau-Desvoidy, 1978); Gekko Smithii Gray, 1842; Gekko subpalmatus (Günther,
1830; Calliphora vomitoria (Linnaeus, 1758); Lucilia caesar 1864); Gekko swinhonis Günther 1864; Gekko vittatus Hout-
(Linnaeus, 1758), Syrphidae: Episyrphus balteatus (De Geer, tuyn, 1782; Hemidactylus frenatus Schlegel, 1836; Hemidactylus
1776); Eristalis tenax (Linnaeus, 1758); Myathropa florea (Lin- turcicus (Linnaeus, 1758); Lepidodactylus lugubris (Duméril &
naeus, 1758); Sphaerophoria scripta (Linnaeus, 1758); Syrphus Bibron, 1836); Lepidodactylus pumilus (Boulenger, 1885); Phel-
ribesii (Linnaeus, 1758); Volucella pellucens (Linnaeus, 1758), suma dubia (Boettger, 1881); Phelsuma grandis Gray, 1870;
Tabanidae: Tabanus spec Linnaeus, 1758, Tachinidae: Tachina Phelsuma laticauda (Boettger, 1880); Rhoptropus afer Peters,
fera (Linnaeus, 1761) 1869; Rhoptropus barnardi Hewitt, 1926; Rhoptropus biporo-
sus FitzSimons, 1957; Rhoptropus boultoni Schmidt, 1933;
Hemiptera, Aphididae: Aphis fabae Scopoli, 1763; Megoura
Rhoptropus bradfieldi Hewitt, 1935; Rhoptropus cf biporosus
viciae Buckton, 1876, Cicadellidae: Aphrodes sp. Curtis, 1833;
(Fitzsimons,1957); Rhoptropus diporus Haacke, 1965, Scinci-
Eupteryx aurata (Linnaeus, 1758), Coreidae: Coreus margina-
dae: Prasinohaema virens Peters, 1881; Prasinohaema pre-
tus (Linnaeus, 1758); Gonocerus acuteangulatus (Goeze, 1778);
hensicauda (Loveridge, 1945); Prasinohaema flavipes (Parker,
Leptoglossus occidentalis Heidemann, 1910, Delphacidae: Asir-
1936); Lipinia leptosoma (Brown & Fehlmann, 1958)
aca clavicornis (Fabricius, 1775); Javesella pellucida (Fabri-
cius, 1794); Ribautodelphax spec (Ribaut, 1953); Stenocranus
minutus (Fabricius, 1787), Heterogastridae: Heterogaster ur-
ticae (Fabricius, 1775), Miridae: Dicyphus errans (Wolff, 1804); References
Lygocoris pabulinus (Linnaeus, 1761), Pentatomidae: Aelia
acuminata (Linnaeus, 1758); Palomena prasina (Linnaeus, [1] Gould SJ (2002) The structure of evolutionary theory.
1761), Triozidae: Trioza urticae (Linnaeus, 1758) Harvard University Press.
Hymenoptera, Formicidae: Atta cephalotes (Linnaeus, 1758);
[2] Taylor G, Thomas A (2014) Evolutionary biomechanics:
Atta colombica (Guérin-Méneville, 1844); Camponotus schmitzi
selection, phylogeny, and constraint. Oxford University
Stärcke, 1933; Myrmica scabrinodis Nylander, 1846; Oecophylla
Press.
smaragdina Fabricius, 1775; Polyrhachis dives Smith, 1857,
Vespidae: Vespa crabro Linnaeus, 1758
[3] McMahon T (1973) Size and shape in biology: Elastic
Lepidoptera, Tortricidae: Cydia pomonella (Linnaeus, 1758) criteria impose limits on biological proportions, and con-
Mantodea, Mantidae: Stagmomantis theophila Rehn, 1904 sequently on metabolic rates. Science 179: 1201–1204.
Orthoptera, Acrididae: Chorthippus brunneus (Thunberg,
1815); Locusta migratoria manilensis (Linnaeus, 1758), Tettigo- [4] Schmidt-Nielsen K (1975) Scaling in biology: the conse-
niidae: Conocephalus discolor (Thunberg, 1815); Metrioptera quences of size. J Exp Zool 194: 287–307.
roeselii (Hagenbach, 1822)
Phasmatodea, Bacillidae: Heteropteryx dilatata (Parkinson, [5] McMahon TA, Bonner JT, Freeman W (1983) On size
1798), Diapheromeridae: Carausius morosus Sinety, 1901; and life. Scientific American Library New York.
Clonaria conformans (Brunner, 1907), Heteropterygidae: Tra-
chyaretaon carmelae Lit & Eusebio, 2005, Phasmatidae: Eu- [6] Schmidt-Nielsen K (1984) Scaling: why is animal size so
rycantha calcarata (Lucas, 1869); Medauroidea extradentata important? Cambridge University Press.
Brunner, 1907; Ramulus spec Saussure, 1862; Sceptrophasma
hispidulum Wood-Mason, 1873 [7] LaBarbera M (1990) Principles of design of fluid transport
Raphidioptera, Raphidiidae: Phaeostigma notatum (Fabri- systems in zoology. Science 249: 992–1000.

8
 bioRxiv preprint doi: https://doi.org/10.1101/033845; this version posted January 18, 2016. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.

[8] Weibel ER (1991) Fractal geometry: a design principle [26] Beutel RG, Gorb SN (2001) Ultrastructure of attachment
for living organisms. Am J Physiol Lung Cell Mol Physiol specializations of Hexapods (Arthropoda): Evolutionary
261: 361–369. patterns inferred from a revised ordinal phylogeny. J Zool
Syst Evol Res 39: 177–207.
[9] West GB, Brown JH, Enquist BJ (1999) The fourth di-
mension of life: fractal geometry and allometric scaling of [27] Gamble T, Greenbaum E, Jackman TR, Russell AP,
organisms. Science 284: 1677–1679. Bauer AM (2012) Repeated origin and loss of adhesive
toepads in geckos. PLoS One 7: e39429.
[10] Alexander R, Jayes A, Maloiy G, Wathuta E (1979)
Allometry of the limb bones of mammals from shrews [28] Wolff JO, Nentwig W, Gorb SN (2013) The great silk
(Sorex) to elephant (Loxodonta). J Zool 189: 305–314. alternative: Multiple co-evolution of web loss and sticky
hairs in spiders. PLoS One 8: e62682.
[11] Biewener AA (1989) Scaling body support in mammals:
limb posture and muscle mechanics. Science 245: 45–48. [29] Johnson MK, Russell AP (2009) Configuration of the setal
fields of Rhoptropus (gekkota: Gekkonidae): functional,
[12] Autumn K, Niewiarowski PH, Puthoff JB (2014) Gecko evolutionary, ecological and phylogenetic implications of
adhesion as a model system for integrative biology, inter- observed pattern. J Anat 214: 937–955.
disciplinary science, and bioinspired engineering. Annu
Rev Ecol Evol Syst 45: 445-470. [30] Higham TE, Birn-Jeffery AV, Collins CE, Hulsey CD,
Russell AP (2014) Adaptive simplification and the evolu-
[13] Jagota A, Hui C (2011) Adhesion, friction, and com- tion of gecko locomotion: Morphological and biomechani-
pliance of bio-mimetic and bio-inspired structured inter- cal consequences of losing adhesion. PNAS 112: 809–814.
faces. Mat Sci Eng R 72: 253–292.
[31] Schmidt-Nielsen K (1970) Energy metabolism, body size,
[14] Bartlett M, Croll A, King D, Paret B, Irschick D, et al. and problems of scaling. Fed Proc 29: 1524–1532.
(2012) Looking beyond fibrillar features to scale gecko-like
adhesion. Adv Mater 24: 1078–83. [32] Powell GL, Russell AP (1992) Locomotor correlates of
ecomorph designation in Anolis: an examination of three
[15] Hawkes EW, Eason EV, Asbeck AT, Cutkosky MR (2013) sympatric species from Jamaica. Can J Zool 70: 725–739.
The gecko’s toe: scaling directional adhesives for climbing
applications. IEEE/ASME Trans Mechatronics 18: 518– [33] Du Bois D, Du Bois EF (1916) Clinical calorimetry: tenth
526. paper a formula to estimate the approximate surface area
if height and weight be known. Arch Intern Med 17: 863–
[16] Labonte D, Federle W (2015) Scaling and biomechanics 871.
of surface attachment in climbing animals. Phil Trans R
Soc B 370: 20140027. [34] Smith JM, Barnes WJP, Downie J, Ruxton G (2006) Ad-
hesion and allometry from metamorphosis to maturation
[17] Pagel M (1999) Inferring the historical patterns of biolog- in hylid tree frogs: a sticky problem. J Zool 270: 372–383.
ical evolution. Nature 401: 877–884.
[35] Hanna G, Barnes WJP (1991) Adhesion and detachment
[18] Egset C, Hansen T, Le Rouzic A, Bolstad G, Rosenqvist of the toe pads of tree frogs. J Exp Biol 155: 103–125.
G, et al. (2012) Artificial selection on allometry: change
in elevation but not slope. J Evol Biol 25: 938–948. [36] Barnes WJP, Oines C, Smith J (2006) Whole animal mea-
surements of shear and adhesive forces in adult tree frogs:
[19] Pelabon C, Firmat C, Bolstad GH, Voje KL, Houle D, insights into underlying mechanisms of adhesion obtained
et al. (2014) Evolution of morphological allometry. Ann from studying the effects of size and scale. J Comp Phys-
NY Acad Sci 1320: 58–75. iol A 192: 1179–1191.

[20] Macrini TE, Irschick DJ, Losos JB (2003) Ecomorphologi- [37] Smith JM, Barnes WJP, Downie JR, Ruxton GD (2006)
cal differences in toepad characteristics between mainland Structural correlates of increased adhesive efficiency with
and island anoles. J Herpetol 37: 52–58. adult size in the toe pads of hylid tree frogs. J Comp
Physiol A 192: 1193–1204.
[21] Betz O (2003) Structure of the tarsi in some Stenus
species (Coleoptera, Staphylinidae): External morphol- [38] Crawford N, Endlein T, Barnes WJP (2012) Self-cleaning
ogy, ultrastructure, and tarsal secretion. J Morphol 255: in tree frog toe pads; a mechanism for recovering from
24–43. contamination without the need for grooming. J Exp Biol
215: 3965–3972.
[22] Wolff JO, Gorb SN (2014) Adhesive foot pads-an adapta-
tion to climbing? An ecological survey in hunting spiders. [39] Arzt E, Gorb S, Spolenak R (2003) From micro to nano
Zoology 118: 1–7. contacts in biological attachment devices. PNAS 100:
10603–10606.
[23] Russell AP, Higham TE (2009) A new angle on clinging
in geckos: incline, not substrate, triggers the deployment [40] Peattie AM, Full RJ (2007) Phylogenetic analysis of the
of the adhesive system. ProcR Soc B 276: 3705–3709. scaling of wet and dry biological fibrillar adhesives. PNAS
104: 18595–18600.
[24] Collins CE, Russell AP, Higham TE (2014) Subdigital
adhesive pad morphology varies in relation to structural [41] Gorb S, Gorb E, Kastner V (2001) Scale effects on the
habitat use in the Namib Day Gecko. Funct Ecol 29: attachment pads and friction forces in syrphid flies. J
66–77. Exp Biol 204: 1421–1431.

[25] Düllman W, Trüb L (1997) Biology of amphibians. Johns [42] Federle W (2006) Why are so many adhesive pads hairy?
Hopkins University Press, 2nd edition. J Exp Biol 209: 2611–2621.

9
 bioRxiv preprint doi: https://doi.org/10.1101/033845; this version posted January 18, 2016. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.

[43] Arnold SJ (1983) Morphology, performance and fitness. [61] Frantsevich L, Gorb S (2004) Structure and mechanics
Am Zool 23: 347–361. of the tarsal chain in the hornet, Vespa crabro (Hy-
menoptera: Vespidae): implications on the attachment
[44] Roth L, Willis E (1952) Tarsal structure and climbing mechanism. Arthropod Struct Dev 33: 77 – 89.
ability of cockroaches. J Exp Zool 119: 483–517.
[62] Zahn M (2006) Allometrie der Hafthaarmorphologie bei
[45] Emerson S, Diehl D (1980) Toe pad morphology and Arthropoden. Master’s thesis, Universität Würzburg.
mechanisms of sticking in frogs. Biol J Linn Soc 13: 199–
216. [63] Bohn HF (2007) Biomechanik von Insekten-Pflanzen-
Interaktionen bei Nepenthes-Kannenpflanzen. Ph.D. the-
[46] Stork N (1980) A scanning electron microscope study of sis, Julius-Maximilians-Universität Würzburg.
tarsal adhesive setae in the Coleoptera. Zool J Linn Soc
68: 173–306. [64] Voigt D, Gorb E, Gorb S (2007) Plant surface-bug interac-
tions: Dicyphus errans stalking along trichomes. Arthro-
[47] Green D, Alberch P (1981) Interdigital webbing and skin pod Plant Interact 1: 221–243.
morphology in the neotropical salamander genus Boli-
toglossa (Amphibia; Plethodontidae). J Morphol 170: [65] Clemente CJ, Federle W (2008) Pushing versus pulling:
273–282. division of labour between tarsal attachement pads in
cockroaches. Proc R Soc B 275: 1329–1336.
[48] Walker G, Yulf AB, Ratcliffe J (1985) The adhesive or-
gan of the blowfly, Calliphora vomitoria: a functional ap- [66] Drechsler P (2008) Mechanics of adhesion and friction
proach (Diptera: Calliphoridae). J Zool 205: 297–307. in stick insects and tree frogs. Ph.D. thesis, Julius-
Maximilians-Universität Würzburg.
[49] Bauer AM, Good D (1986) Scaling of scansorial surface
area in the genus Gekko. In: Roček Z, editor, Studies in [67] Niewiarowski PH, Lopez S, Ge L, Hagan E, Dhinojwala
herpetology, Prague: Charles University. pp. 363–366. A (2008) Sticky gecko feet: the role of temperature and
humidity. PLoS One 3: e2192.
[50] Ishii S (1987) Adhesion of a leaf-feeding ladybird Epi-
lachna vigintioctomaculata (Coleoptera, Coccinellidae) [68] Frantsevich L, Ji A, Dai Z, Wang J, Frantsevich L, et al.
on a vertically smooth surface. Appl Entomol Zool 22: (2008) Adhesive properties of the arolium of a lantern-
222–228. fly, Lycorma delicatula (Auchenorrhyncha, Fulgoridae).
J Insect Physiol 54: 818–827.
[51] Lees AD, Hardie J (1988) The organs of adhesion in the
aphid Megoura viciae. J Exp Biol 136: 209–228. [69] Al Bitar L, Voigt D, Zebitz C, Gorb S (2009) Tarsal
morphology and attachment ability of the codling moth
[52] Dixon AFG, Croghan P, Gowing R (1990) The mechanism
Cydia pomonella L.(Lepidoptera, Tortricidae) to smooth
by which aphids adhere to smooth surfaces. J Exp Biol
surfaces. J Insect Physiol 55: 1029–1038.
152: 243–253.
[70] Bullock JMR, Federle W (2009) Division of labour and
[53] Walker G (1993) Adhesion to smooth surfaces by insects–
sex differences between fibrillar, tarsal adhesive pads in
a review. Int J Adhes Adhes 13: 3–7.
beetles: effective elastic modulus and attachment perfor-
[54] Irschick DJ, Austin CC, Petren K, Fisher RN, Losos JB, mance. J Exp Biol 212: 1876–1888.
et al. (1996) A comparative analysis of clinging ability
[71] Geiselhardt SF, Geiselhardt S, Peschke K (2009) Compar-
among pad-bearing lizards. Biol J Linn Soc 59: 21–35.
ison of tarsal and cuticular chemistry in the leaf beetle
[55] Eisner T, Aneshansley D (2000) Defense by foot adhesion Gastrophysa viridula (Coleoptera: Chrysomelidae) and
in a beetle (Hemisphaerota cyanea). PNAS 97: 6568– an evaluation of solid-phase microextraction and solvent
6573. extraction techniques. Chemoecology 19: 185–193.

[56] Federle W, Rohrseitz K, Hölldobler B (2000) Attachment [72] Lüken D, Voigt D, Gorb S, Zebitz C (2009) Die
forces of ants measured with a centrifuge: better ’wax- Tarsenmorphologie und die Haftfähigkeit des Schwarzen
runners’ have a poorer attachment to a smooth surface. Batatenkäfers Cylas puncticollis (Boheman) auf glat-
J Exp Biol 203: 505–512. ten oberflächen mit unterschiedlichen physiko-chemischen
eigenschaften. Mitt Dtsch Ges allg angew Entomol 17:
[57] Gorb SN, Beutel RG, Gorb EV, Jiao Y, Kastner V, et al. 109–113.
(2002) Structural design and biomechanics of friction-
based releasable attachment devices in insects. Integr [73] Webster NB, Johnson MK, Russell AP (2009) Ontoge-
Comp Biol 42: 1127–1139. netic scaling of scansorial surface area and setal dimen-
sions of Chondrodactylus bibronii (Gekkota: Gekkonidae):
[58] Kesel A, Martin A, Seidl T (2004) Getting a grip on spider testing predictions derived from cross-species comparisons
attachment: an afm approach to microstructure adhesion of gekkotans. Acta Zool 90: 18–29.
in arthropods. Smart Mater Struct 13: 512.
[74] Gorb EV, Hosoda N, Miksch C, Gorb SN (2010) Slippery
[59] Elstrott J, Irschick DJ (2004) Evolutionary correlations pores: anti-adhesive effect of nanoporous substrates on
among morphology, habitat use and clinging performance the beetle attachment system. J R Soc Interface 7: 1571–
in caribbean Anolis lizards. Biol J Linn Soc 83: 389–398. 1579.

[60] Federle W, Baumgartner W, Hölldobler B (2004) Biome- [75] Riskin D, Racey P (2010) How do sucker footed bats hold
chanics of ant adhesive pads: frictional forces are rate- on, and why do they roost head up? Biol J Linn Soc 99:
and temperature dependent. J Exp Biol 206: 67–74. 233–240.

10
 bioRxiv preprint doi: https://doi.org/10.1101/033845; this version posted January 18, 2016. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.

[76] Varenberg M, Pugno N, Gorb S (2010) Spatulate struc- [93] Bullock JMR, Federle W (2011) Beetle adhesive hairs dif-
tures in biological fibrillar adhesion. Soft Matter 6: 3269– fer in stiffness and stickiness: in vivo adhesion measure-
3272. ments on individual setae. Naturwissenschaften 98: 381–
387.
[77] Orchard MJ, Kohonen M, Humphries S (2012) The influ-
ence of surface energy on the self-cleaning of insect adhe- [94] Peattie AM, Dirks JH, Henriques S, Federle W (2011)
sive devices. J Exp Biol 215: 279–286. Arachnids secrete a fluid over their adhesive pads. PLoS
One 6: e20485.
[78] Orchard MJ (2012) The functional morphology of insect
adhesive devices and its implications for ecology. Ph.D. [95] Arnold J (1974) Adaptive features on the tarsi of cock-
thesis, University of Hull. roaches (Insecta: Dictyoptera). Insect Morphol Embryol
3: 317–334.
[79] Voigt D, Schweikart A, Fery A, Gorb S (2012) Leaf beetle
attachment on wrinkles: isotropic friction on anisotropic [96] Frazier SF, Larsen GS, Neff D, Quimby L, Carney M,
surfaces. J Exp Biol 215: 1975–1982. et al. (1999) Elasticity and movements of the cockroach
tarsus in walking. J Comp Physiol 185: 157–172.
[80] Wolff JO, Gorb SN (2012) Surface roughness effects
on attachment ability of the spider Philodromus dispar [97] Beutel R, Gorb S (2006) A revised interpretation of at-
(Araneae, Philodromidae). J Exp Biol 215: 179–184. tachment structures in Hexapoda with special emphasis
on Mantophasmatodea. Arthropod Syst Phylogeny 64:
[81] Anyon MJ (2013) A Multi-Disciplinary Study of Insect
3–25.
Adhesion: Functional Biomechanics and Applications.
Ph.D. thesis, University of Hull. [98] Eberhard MJ, Pass G, Picker MD, Beutel R, Predel R,
et al. (2009) Structure and function of the arolium of
[82] Endlein T, Barnes WJP, Samuel DS, Crawford NA, Biaw
Mantophasmatodea (Insecta). J Morphol 270: 1247–
AB, et al. (2013) Sticking under wet conditions: The re-
1261.
markable attachment abilities of the torrent frog, Staurois
guttatus. PloS One 8: e73810. [99] Clemente C, Dirks J, Barbero D, Steiner U, Federle
W (2009) Friction ridges in cockroach climbing pads:
[83] Labonte D, Federle W (2013) Functionally different pads
anisotropy of shear stress measured on transparent, mi-
on the same foot allow control of attachment: stick in-
crostructured substrates. J Comp Physiol A 195: 805–
sects have load-sensitive ‘heel’ pads for friction and shear-
814.
sensitive ‘toe’ pads for adhesion. PLoS One 8: e81943.
[100] Labonte D, Williams J, Federle W (2014) Surface con-
[84] Crandell KE, Herrel A, Sasa M, Losos JB, Autumn K
tact and design of fibrillar ‘friction pads’ in stick insects
(2014) Stick or grip? Co-evolution of adhesive toepads
(carausius morosus): mechanisms for large friction coef-
and claws in Anolis lizards. Zoology 117: 363–369.
ficients and negligible adhesion. J R Soc Interface 11:
[85] Grohmann C, Blankenstein A, Koops S, Gorb SN (2014) 20140034.
Attachment of Galerucella nymphaeae (Coleoptera,
[101] Gorb S, Scherge M (2000) Biological microtribology:
Chrysomelidae) to surfaces with different surface energy.
anisotropy in frictional forces of orthopteran attachment
J Exp Biol 217: 4213–4220.
pads reflects the ultrastructure of a highly deformable ma-
[86] Lapinski W, Walther P, Tschapka M (2015) Morphol- terial. Proc R Soc B 267: 1239–1244.
ogy reflects microhabitat preferences in an assemblage of
[102] Grohmann C, Henze MJ, Nørgaard T, Gorb SN (2015)
neotropical wandering spiders. Zoomorphology 134: 219–
Two functional types of attachment pads on a single foot
236.
in the Namibia bush cricket Acanthoproctus diadematus
[87] Luff M (2007) The Carabidae (ground beetles) of Britain (Orthoptera: Tettigoniidae). Proc R Soc B 282.
and Ireland. RES handbooks for the identification of
[103] Drotlef DM, Appel E, Peisker H, Dening K, del Campo A,
British Insects, volume 4. Field Studies Council, Shrews-
et al. (2014) Morphological studies of the toe pads of the
bury.
rock frog, Staurois parvus (family: Ranidae) and their rel-
[88] Biedermann R, Niedringhaus R (2009) The plant- evance to the development of new biomimetically inspired
and leafhoppers of Germany: identification key to reversible adhesives. Interface Focus 5: 20140036.
all species. Scheeßel: Wissenschaftlich Akademischer
Buchvertrieb–Fründ. [104] Emerson SB S (1991) The ecomorphology of bornean tree
frogs (family Rhacophoridae). Zool J Linn Soc 101: 337–
[89] Kunz G, Nickel H, Niedringhaus R (2011) Fotoatlas 357.
der Zikaden Deutschlands. Scheeßel: Wissenschaftlich
Akademischer Buchvertrieb–Fründ. [105] Voigt D, Schuppert J, Dattinger S, Gorb S (2008) Sex-
ual dimorphism in the attachment ability of the colorado
[90] Schneider C, Rasband W, Eliceiri K (2012) NIH Image potato beetle Leptinotarsa decemlineata (Coleoptera:
to ImageJ: 25 years of image analysis. Nat Methods 9: Chrysomelidae) to rough substrates. J Insect Physiol 54:
671–675. 765–776.

[91] Bullock JMR, Drechsler P, Federle W (2008) Comparison [106] Al Bitar L, Voigt D, Zebitz CP, Gorb SN (2010) Attach-
of smooth and hairy attachment pads in insects: fric- ment ability of the codling moth Cydia pomonella L. to
tion, adhesion and mechanisms for direction-dependence. rough substrates. J Insect Physiol 56: 1966–1972.
J Exp Biol 211: 3333–3343.
[107] Labonte D, Federle W (2015) Rate-dependence of ‘wet’
[92] Autumn K, Gravish N (2008) Gecko adhesion: evolution- biological adhesives and the function of the pad secretion
ary nanotechnology. Phil Trans R Soc A 366: 1575–1590. in insects. Soft Matter 11: 8661–8673.

11
 bioRxiv preprint doi: https://doi.org/10.1101/033845; this version posted January 18, 2016. The copyright holder for this preprint (which
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
available under aCC-BY 4.0 International license.

[108] Schluter D (1996) Adaptive radiation along genetic lines [126] Warton DI, Wright IJ, Falster DS, Westoby M (2006)
of least resistance. Evolution 50: 1766–1774. Bivariate line-fitting methods for allometry. Biol Rev 81:
259–291.
[109] Pyron RA, Wiens JJ (2011) A large-scale phylogeny of
Amphibia including over 2800 species, and a revised clas- [127] Hansen TF, Bartoszek K (2012) Interpreting the evolu-
sification of extant frogs, salamanders, and caecilians. Mol tionary regression: the interplay between observational
Phylogenet Evol 61: 543–583. and biological errors in phylogenetic comparative studies.
Syst Biol 61: 413–425.
[110] Pyron RA, Burbrink FT, Wiens JJ (2013) A phylogeny
and revised classification of Squamata, including 4161 [128] Revell LJ (2013) Two new graphical methods for mapping
species of lizards and snakes. BMC Evol Biol 13: 93. trait evolution on phylogenies. Methods Ecol Evol 4: 754–
759.
[111] Misof B, Liu S, Meusemann K, Peters RS, Donath A,
et al. (2014) Phylogenomics resolves the timing and pat-
tern of insect evolution. Science 346: 763–767.

[112] Grandcolas P (1996) The phylogeny of cockroach families:

a cladistic appraisal of morpho-anatomical data. Can J
Zool 74: 508–527.

[113] Bocak L, Barton C, Crampton-Platt A, Chesters D,

Ahrens D, et al. (2014) Building the Coleoptera tree-of-
life for > 8000 species: composition of public DNA data
and fit with linnean classification. Syst Entomol 39: 97–
110.

[114] Wiegmann BM, Trautwein MD, Winkler IS, Barr NB,

Kim JW, et al. (2011) Episodic radiations in the fly tree
of life. PNAS 108: 5690–5695.

[115] Hua J, Li M, Dong P, Cui Y, Xie Q, et al. (2008) Com-

parative and phylogenomic studies on the mitochondrial
genomes of Pentatomomorpha (Insecta: Hemiptera: Het-
eroptera). BMC genomics 9.

[116] Cryan JR, Urban JM (2012) Higher-level phylogeny of

the insect order Hemiptera: is Auchenorrhyncha really
paraphyletic? Syst Entomol 37: 7–21.

[117] Astruc C, Julien J, Errard C, Lenoir A (2004) Phylogeny

of ants (Formicidae) based on morphology and DNA se-
quence data. Mol Phylogenet Evol 31: 880–893.

[118] tolweborg (accessed March 2015). Tree of Life Project.

[119] Hansen TF, Pienaar J, Orzack SH (2008) A comparative

method for studying adaptation to a randomly evolving
environment. Evolution 62: 1965–1977.

[120] Voje KL, Hansen TF (2013) Evolution of static allome-

tries: adaptive change in allometric slopes of eye span in
stalk-eyed flies. Evolution 67: 453–467.

[121] Paradis E (2013) Molecular dating of phylogenies by like-

lihood methods: a comparison of models and a new in-
formation criterion. Mol Phylogenet Evol 67: 436–444.

[122] Revell LJ (2010) Phylogenetic signal and linear regression

on species data. Methods Ecol Evol 1: 319–329.

[123] Paradis E, Claude J, Strimmer K (2004) APE: Analyses of

phylogenetics and evolution in r language. Bioinformatics
20: 289–290.

[124] Revell LJ (2012) phytools: an R package for phylogenetic

comparative biology (and other things). Methods Ecol
Evol 3: 217–223.

[125] Harvey PH, Pagel MD (1991) The comparative method

in evolutionary biology, volume 239. Oxford: Oxford Uni-
versity Press.

12