Biol. Rev. (2010), pp. 000–000.
doi: 10.1111/j.1469-185X.2010.00132.x
1
Mechanisms of temporary adhesion in benthic
animals
D. Dodou1∗ , P. Breedveld1 , J. C. F. de Winter1 , J. Dankelman1 and J. L. van Leeuwen2
1 Department
of BioMechanical Engineering, Faculty of Mechanical, Maritime and Materials Engineering, Delft University of Technology,
The Netherlands
2 Experimental Zoology Group, Wageningen Institute of Animal Sciences, Wageningen University, The Netherlands
(Received 30 June 2009; revised 25 January 2010; accepted 28 January 2010)
ABSTRACT
Adhesive systems are ubiquitous in benthic animals and play a key role in diverse functions such as locomotion,
food capture, mating, burrow building, and defence. For benthic animals that release adhesives, surface and material
properties and external morphology have received little attention compared to the biochemical content of the adhesives.
We address temporary adhesion of benthic animals from the following three structural levels: (a) the biochemical content
of the adhesive secretions, (b) the micro- and mesoscopic surface geometry and material properties of the adhesive
organs, and (c) the macroscopic external morphology of the adhesive organs. We show that temporary adhesion of
benthic animals is affected by three structural levels: the adhesive secretions provide binding to the substratum at a
molecular scale, whereas surface geometry and external morphology increase the contact area with the irregular and
unpredictable profile of the substratum from micro- to macroscales. The biochemical content of the adhesive secretions
differs between abiotic and biotic substrata. The biochemistry of the adhesives suitable for biotic substrata differentiates
further according to whether adhesion must be activated quickly (e.g. as a defensive mechanism) or more slowly (e.g.
during adhesion of parasites). De-adhesion is controlled by additional secretions, enzymes, or mechanically. Due to
deformability, the adhesive organs achieve intimate contact by adapting their surface profile to the roughness of the
substratum. Surface projections, namely cilia, cuticular villi, papillae, and papulae increase the contact area or penetrate
through the secreted adhesive to provide direct contact with the substratum. We expect that the same three structural
levels investigated here will also affect the performance of artificial adhesive systems.
Key words: benthic animals, temporary adhesion, adhesive secretions, biochemical content, surface geometry, external
morphology.
CONTENTS
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
II. Biochemical content . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(1) Adhesion to abiotic substrata . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(2) Adhesion to biotic substrata . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(a) Slow adhesion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(b) Quick adhesion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(3) De-adhesion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(a) Duo-gland systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(b) Mono-gland systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(4) Diversity and convergence in the biochemical content of adhesive systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
III. Micro- and mesoscopic surface geometry and material properties . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(1) Material deformability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(2) Surface-projecting structures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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* Address for correspondence: Tel: +31 15 278 4221; E-mail: [email protected]
Biological Reviews (2010) 000–000 © 2010 The Authors. Journal compilation © 2010 Cambridge Philosophical Society
D. Dodou and others
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IV.
V.
VI.
VII.
VIII.
(a) Cilia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(b) Cuticular villi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(c) Papillae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(d) Papulae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Macroscopic external morphology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(1) Low-curvature morphologies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(a) Extended low-curvature morphologies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(b) Localised low-curvature morphologies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(2) Projecting morphologies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(a) Multiple-feet projecting morphologies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
( i ) Tube feet . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
( ii ) Podia in sponges . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
( iii ) Arms for free walking . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
( iv ) Threads for restricted walking . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(b) Branched-feet projecting morphologies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
( i ) Digitate podia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
( ii ) Peltate and pelto-digitate tentacles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
( iii ) Pinnate tentacles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(c) Tentacular projecting morphologies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
( i ) Autotomising tentacles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
( ii ) Retracting tentacles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(1) Biological research . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(2) Comparative studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(3) Biomimetic potential . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
I. INTRODUCTION
Benthic animals employ strong temporary attachment
mechanisms for a variety of actions, such as locomotion,
food capture, mating, burrow building, and defence, to
withstand water currents that would otherwise sweep them
away from their working environment. Some benthic animals
use clamps, spines, or suction to achieve grip, whereas
others secrete adhesives. The adhesives of benthic animals
can be permanent, transitory, or temporary (Flammang,
1996; Scherge & Gorb, 2001; Tyler, 1988). Permanent
adhesives are secreted as fluids, which then solidify to
form a cement (as in barnacles). Transitory adhesives allow
movement while sticking: The animal interposes an adhesive
film between its body and the substratum and creeps along
it (as in gastropods). Temporary adhesives, which are the
focus herein, allow repetitive stick-unstick cycles (as in
echinoderms). In practice, the distinction between transitory
and temporary adhesion is not clear-cut (Flammang, 2006)
and the operating time scales of these two modes of adhesion
are overlapping (Gorb, 2008).
In terrestrial environments, spiders and geckos are able
to cling to surfaces very strongly without claws and
without releasing adhesives. These animals possess hairy
attachment systems and their grip relies entirely on the microand mesoscopic surface geometry (relief) and macroscopic
external morphology (shape) of their exoskeleton or footpads
(e.g. Arzt, Gorb & Spolenak, 2003; Peressadko & Gorb,
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2004). Dry adhesion is the effect of van der Waals forces
between the footpad or exoskeleton of the animal and the
substratum. Theories are being developed that attempt to
describe the adhesion of terrestrial animals as a function
of either the surface geometry and external morphology of
their attachment systems (Arzt et al., 2003; Peressadko &
Gorb, 2004) or their phylogenetic characteristics (Peattie &
Full, 2007).
For benthic animals that release temporary adhesives,
the roles of surface geometry and external morphology
in adhesion have received little attention compared to
the biochemical content of the adhesives; attempts to
develop a theoretical framework describing the mechanisms
of adhesion of these animals remain limited. A recent
study by Santos et al. (2005a) showed that the adhesive
footpads of echinoderms deform in a viscoelastic manner to
match the roughness of the substratum. Surface-projecting
structures such as cilia and papillae have been studied
extensively, but predominantly in relation to the secretory
and sensory cells present underneath the epidermis. Some
have related the external morphology of the adhesive organs
in sea stars (Asteroidea) to habitat demands (Blake, 1989;
Flammang, 2006; Santos et al., 2005b), but others have
argued that a consistent relationship exists between the
external morphology of these organs and taxonomic position
(Vickery & McClintock, 2000).
We review the attachment mechanisms of benthic animals
that release temporary adhesives from three structural
Biological Reviews (2010) 000–000 © 2010 The Authors. Journal compilation © 2010 Cambridge Philosophical Society
Mechanisms of temporary adhesion in benthic animals
levels: (a) the biochemical content of the released adhesives,
(b) the material deformability and the micro- (<10 μm)
and mesoscopic (10–100 μm) surface geometry of the
adhesive organs, and (c) the macroscopic (>100 μm)
external morphology of the adhesive organs (Fig. 1). Within
these structural levels, subcategories are defined specifying
shared mechanisms of adhesion across taxa. The functional
significance of these structural levels is addressed and
perspectives for future biological research as well as the
biomimetic potential of biological adhesion mechanisms are
discussed.
II. BIOCHEMICAL CONTENT
The strength of the bonds between the epithelium of
the adhesive organ and the substratum depends on
the biochemical nature of the adhesive secretions. The
temporary character of the adhesion is controlled either
by the release of de-adhesive secretions or mechanically. We
distinguish between adhesive secretions suitable for abiotic
and for biotic substrata. The latter are further divided into
secretions for slow adhesion (e.g. in parasites) and for quick
adhesion (e.g. during defence). Finally, two mechanisms
of de-adhesion are discussed: duo-gland and mono-gland
systems.
(1) Adhesion to abiotic substrata
All echinoderms examined so far possess tube feet with two
types of non-ciliated secretory (NCS) cells. These enclose
large heterogeneous granules and secrete an adhesive used
for locomotion and anchoring to abiotic substrata, or for
picking up sand particles. The adhesive is present as a thin
film between the cuticle of the tube foot and the substratum
(Thomas & Hermans, 1985). The cuticle consists of an
internal fibrous layer (lower cuticle), a middle layer with
granules (upper cuticle), and an external layer with fine
filaments (fuzzy coat) (Ameye et al., 2000). The fuzzy coat
of echinoderms is particularly thick, approximately 800 nm,
and probably consists of hydrophilic proteoglycans, which
make it gelatinous (Ameye et al., 2000). McKenzie (1988)
suggested that the fuzzy coat is glycocalyx with anti-fouling
properties. The adhesive secretions of echinoderms are a
mixture of proteins and carbohydrates in a ratio of around
2:1 dry weight, with the protein fraction including charged
and polar amino acids and small-side-chain amino acids, and
the carbohydrates mostly in the form of acidic and sulphated
sugars. The secretions also include an inorganic fraction
(possibly consisting of salts from sea water, see Smith &
Morin, 2002) that represents more than 40% of the adhesive
material (Flammang et al., 1998).
The mean normal tenacity (i.e. adhesive yield stress) of
echinoderm adhesives ranges between 59 and 290 kPa for the
sea urchins Arbacia lixula and Paracentrotus lividus, respectively,
as measured by Flammang, Santos & Haesaerts (2005).
These values are comparable to the tenacity of marine
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invertebrates that secrete permanent adhesives, such as
limpets and barnacles (230 kPa for both, as reviewed by
Flammang, 2006). The co-presence of charged and polar
amino acids and small-side-chain amino acids attributes to
these adhesives both high cohesiveness and high adhesive
strength (Flammang, 2006): the charged/polar amino acids
generate ionic and hydrogen bonds with the contact surface,
whereas the small-side-chain amino acids increase the
elasticity of the proteins, allowing the adhesive to sustain
high deformations without rupture. The cohesiveness and
adhesiveness of the secretions are further a trade-off between
the degree of crosslinking and the chain length between the
crosslinks: increasing the degree of crosslinking makes the
material more cohesive but leaves less side chains free for
adhesion, whereas with longer chains a material is more
adhesive but less cohesive. The protein fraction contains
relatively high amounts of glycine, proline, isoleucine, and
cysteine. Cysteine is responsible for intermolecular disulfide
bonds that increase the cohesiveness of an adhesive, and
glycine is characteristic of strong, tightly bound proteins
such as those in silk.
The strength of echinoderm adhesives is further enhanced
by the fact that the released material consists of a spongelike matrix with 3–10 μm holes defined by walls of 0.4
μm thickness, which inhibits the propagation of cracks
and increases its adhesive strength (Flammang et al., 1998)
(Fig. 2A). The spongy appearance is most pronounced in
the thinnest areas of the footprint; when larger quantities
of adhesive are secreted, the footprint exhibits a feltlike appearance (Flammang et al., 1998). For mussels and
barnacles it has been found that proteins are self-organised
to create the porous layer (Wiegemann & Watermann,
2003). For echinoderms less is known about the exact
mechanism underlying the development of their adhesive
matrix. Recently, Hennebert et al. (2008) provided evidence
about the roles of the two types of NCS cells in the
development of the matrix: one type of cell produces a
homogeneous film that covers the substratum and the
other type of cell releases heterogeneous electron-dense
material that expands and fuses into the homogeneous film.
Hennebert et al. (2008) superimposed adhesive pores on the
adhesive matrix and found a match indicating the adhesive
cells possibly form a template for casting the matrix pattern.
Apart from their common general working principle
and gross biochemical similarities, the adhesive secretions
of echinoderms exhibit function- and habitat-related
differentiation at the glandular and cellular level. In
asteroids, species confined to hard rocky substrata have
complex NCS cell granules enclosing a highly organised
core. Soft-substratum-dwelling species, on the other hand,
have granules with a simpler ultrastructure (Engster &
Brown, 1972). A mechanistic explanation of this habitatrelated difference is still to be found. In sea urchins,
the epidermal cells are flask-shaped in coronal podia
and cylindrical in peristomeal podia. This differentiation
is possibly function-related: stronger adhesion is required
for coronal podia anchoring to a substratum than
Biological Reviews (2010) 000–000 © 2010 The Authors. Journal compilation © 2010 Cambridge Philosophical Society
Biological Reviews (2010) 000–000 © 2010 The Authors. Journal compilation © 2010 Cambridge Philosophical Society
Slow
Quick
Adhesion
for biotic
substrata
Duogland
systems
Monogland
systems
De-adhesion
10 μm
Mesoscale
Material deformability
Cilia
Cuticular
villi
Papillae
Papulae
Surface-projecting structures
Low-curvature
morphologies
Extended
Localised
low-curvature low-curvature
morphologies morphologies
100 μm
Micro/mesoscopic surface geometry and material properties
Microscale
Macroscale
Disc- Knob- Penicending ending illate
Tube feet
Peltate
Tentacular projecting morphologies
Pinnate Autoto- Retracting
mising
Branched-feet
projecting morphologies
Podia in Arms for Threads Digitate
sponges free walk- for restricing
ted walking
Multiple-feet
projecting morphologies
Projecting morphologies
Macroscopic external morphology
INCREASE CONTACT AREA
Fig. 1. The proposed structural levels of temporary adhesion mechanisms. The grey surfaces represent the adhesive areas in the line drawings. The illustrations are not to
scale.
Adhesion
for abiotic
substrata
Adhesion
Biochemical content
Molecular scale
PROVIDE MOLECULAR BINDING
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D. Dodou and others
Mechanisms of temporary adhesion in benthic animals
A
D
B
E
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C
F
G
Fig. 2. (A) Adhesive footprint of the asteroid Asterias rubens (Flammang et al., 1998). (B) Adhesive footprint of the platyhelminth
Troglocephalus rhinobatidis (Hamwood et al., 2002). Note the similar spongy structure of (A) and (B). (C) Cuvierian tubules of the
holothuroid Holothuria forskali (lower left) immobilising a crab (upper right) (scale not reported in the original) (Flammang et al., 2002).
(D, E) Duo-gland adhesive system in A. rubens. Longitudinal sections before attachment (D) and after detachment (E) CS: ciliated
secretory cell, CU: cuticle, FC: fuzzy coat, NCS1: type 1 non-ciliated secretory cell, NCS2: type 2 non-ciliated secretory cell, P: pore,
SCC: subcuticular cilium, SG: secretory granule (Flammang et al., 2005). (F, G) Anterior adhesive area in T. rhinobatidis. Longitudinal
sections with everted duct endings (arrows) during attachment (F) and with retracted duct endings (arrows) after detachment (G)
A: adhesive, I: integument, ES: electron-dense spheroidal secretions, RS: rod-shaped secretions (Whittington et al., 2004). The insets
correspond to the structural level illustrations in Fig. 1.
for peristomeal podia wrapping particles (Flammang &
Jangoux, 1993). A unique adhesive system has been
found in the tentacles of the holothurian Leptosynapta sp.
(Holothurioidea, Echinodermata) (McKenzie, 1988). The
tentacles of Leptosynapta sp. contain secreting goblet cells
not found in any other dendrochirote or aspidochirote
holothurian (Bouland, Massin & Jangoux, 1982; Fankboner,
1978; McKenzie, 1987), and the pH of the secreted mucus is
basic, therefore having weaker de-adhesive properties than
if it had been acidic (Hermans, 1983). Leptosynapta sp. has a
delicate, worm-like apodous morphology and its tentacles are
used to consolidate and lubricate its burrow. The properties
of the adhesive system of Leptosynapta sp. are thus likely
to be related to the lifestyle of this animal, which differs
from that of dendrochirote and aspidochirote holothurians
(McKenzie, 1988).
The arms of the brachiolaria larvae of sea stars carry adhesive cells that contain molecules similar to those found in the
adhesive system of the adult sea stars and which are suitable
for attaching to abiotic surfaces during exploration (Haesaerts
et al., 2005a). Other benthic animals possessing adhesive systems suitable for abiotic substrata include the archiannelids
Protodrilus sp., Saccocirrus sonomacus, and Saccocirrus eroticus
(Martin, 1978), the turbellarian Monocelis cincta (Martin,
1978), several gastrotricha (Tyler & Rieger, 1980), nematoda (Adams & Tyler, 1980), and the cephalopods Euprymna
scolopes and Idiosepius sp. (Von Byern & Klepal, 2006).
(2) Adhesion to biotic substrata
(a) Slow adhesion
Whittington & Cribb (2001) introduced the term ‘‘tissue
adhesion’’ to define adhesion of organisms to biotic substrata
(i.e. living individuals), such as the adhesion of parasitic
organisms to the skin of their hosts. Tissue adhesives
are remarkably strong, able to bond to the current-swept
skin of the host organism. They can be permanent (as in
parasitic barnacles), transitory (as in parasitic gastropods), or
temporary (as in parasitic monogeneans). Here we focus on
the latter type.
Temporary tissue adhesives have been found and
characterised in a number of monogenean (platyhelminth)
parasites, mainly Capsalidae (Hamwood et al., 2002). The
adhesive secretions of the monogenean parasite Entobdella
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D. Dodou and others
6
soleae as well as of other monogeneans such as Troglocephalus
rhinobatidis (Fig. 2B) are similar in appearance to those of
asteroids (Fig. 2A): they have similar amino acid profiles
and are porous, insoluble, spongy, soft, proteinaceous, and
with networks of strands (Hamwood et al., 2002). However,
compared to sea star adhesives, monogenean adhesives
contain neurophysin and keratin, higher concentrations of
glycine and threonine, lower concentrations of isoleucine,
and they lack carbohydrates and lipids. The presence of
keratin is crucial for the toughness of tissue adhesives: keratin
is a tightly folded protein with helices interlinked via disulfide
bonds; when stresses are applied, a domain unfolds, acting
as an effective energy absorber and preventing breakage
of strong bonds in the backbone proteins. Furthermore,
although in both sea stars and monogeneans the adhesives
are stored in rod-shaped bodies, outer membranes of these
bodies show up only in the glue matrix of the monogenean
secretions and not in sea star secretions. Hamwood et al.
(2002) suggested that these structural differences between
monogenean and asteroid adhesives may be critical for the
strong attachment of monogeneans to their living hosts.
A different adhesion mechanism than that in E. solea has
been found in the monocotylidan monogenean Neoheterocotyle
rhinobatidis and Troglocephalus rhinobatidis. Whereas in E. solea
the adhesives are secreted by two permanently exposed
adhesive pads, monocotylids possess anterior apertures.
When these flatworms approach a substratum, they extend
anteriorly to initiate contact and open the apertures so
that the duct endings are everted and secrete an adhesive
(Whittington, Armstrong & Cribb, 2004). When the animal
resumes swimming, the duct endings are retracted into the
apertures (see also Section II.3b).
Cyprids, the last mobile larval form of barnacles, explore
surfaces by using a pair of antennules that are able to attach,
detach, and reattach to a surface, allowing the cyprid to
‘‘walk’’ in a bipedal fashion. Attachment is mediated by the
secretion of a protein (Callow & Callow, 2001; Walker
& Yule, 1984). Recently, Phang et al. (2010) conducted
mechanical testing of the proteins in the cyprid footprint
and found that the individual fibrils of the adhesive exhibit
anisotropic properties: they are interconnected by thin fibres.
It is possible that these fibres act as sacrificial bonds and
fail first, absorbing energy, thereby preventing breakage
of backbone proteins – similar to the spongy material of
echinoderm adhesives described in Section II.1.
(b) Quick adhesion
A small number of benthic animals have systems that release
quick-setting adhesives for capturing prey and immobilise
predators. Such a mechanism is used for prey capture by the
tentilla of Coeloplana bannworthi (Ctenophora, Platyctenida)
(Eeckhaut et al., 1997; see also Franc, 1978) and by the
Cuvierian tubules of sea cucumber species (Endean, 1957;
Flammang, Ribesse & Jangoux, 2002).
Cuvierian tubules are stored in large numbers (200–600
in Holothuria forskali) in the posterior cavity of sea cucumbers
(VandenSpiegel & Jangoux, 1987; VandenSpiegel, Jangoux
& Flammang, 2000). When disturbed by a predator, a sea
cucumber expels 10–20 Cuvierian tubules, which, as soon
as they contact the water, elongate by up to 20 times their
original length (from 2.5 cm to 50 cm; VandenSpiegel &
Jangoux, 1987) and stick to the predator in less than 10 s,
which is considerably quicker than most biological adhesives
(DeMoor et al., 2003) (Fig. 2C).
The mean normal tenacities of Cuvierian tubules vary
between 30 and 135 kPa (DeMoor et al., 2003), which is
towards the low end of the range of tenacities measured
for other temporary adhesives. Quantitative studies on the
amount of adhesive released are missing, but this may be
larger than that of adhesives secreted during functions such
as locomotion, considering that defence is an important but
relatively infrequent activity.
The adhesion of Cuvierian tubules is derived from their
mesothelium, which consists of two layers, an outer protective
layer and an inner one with densely packed granular cells.
When the tubules are expelled from the body and expand,
the outer layer disintegrates exposing the granular cells,
which expel their contents and adhere to the body of the
predator. The material stored in the cells prior to release
is rich in protein and amino acids with low molecular
weight (around 10–19 kDa). The released material includes
proteins with molecular weights ranging between 10 and
220 kDa. The proteins contain amino acids closely related
to those in the stored material suggesting that the proteins in
the secreted material result from polymerisation of the low
molecular weight protein (DeMoor et al., 2003). How this
polymerisation occurs within few seconds upon release of the
protein in water remains unknown.
The adhesive released by Cuvierian tubules is a 3:2 mixture of proteins and carbohydrates and contains a high
proportion of insoluble proteins (DeMoor et al., 2003). The
protein fraction contains a high percentage (more than 70%)
of charged and polar amino acids, but its polarity is relatively low (around 45%) compared to other marine adhesives
(Flammang, 2006). Still the adhesives of Cuvierian tubules
are the most hydrophilic among the marine adhesives investigated so far. The combination of decreased polarity and
increased hydrophilicity in Cuvierian tubules perhaps indicates a trade-off between reduced adhesive strength and
increased activation speed. Although decreased polarity usually relates to decreased hydrophilicity, in marine adhesives
these two properties are not mutually antagonistic (Flammang, 2006), because marine adhesives consist of a mixture
of different proteins. The protein fraction in the adhesive
released by Cuvierian tubules is rich in glycine (DeMoor et al.,
2003), almost matching that in mussel adhesives, whereas
the carbohydrates are in the form of neutral sugars only, not
acidic sugars as in the adhesives used for abiotic substrata.
The inorganic residue is only 11% – considerably less than
the 40% in the adhesives used for abiotic substrata. The high
percentage of carbohydrates as well as the presence of precursor proteins with low molecular weight, which polymerise
upon release, may explain the rapid activation of adhesion
by Cuvierian tubules (Flammang & Jangoux, 2004).
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Mechanisms of temporary adhesion in benthic animals
7
(4) Diversity and convergence in the biochemical
content of adhesive systems
(3) De-adhesion
(a) Duo-gland systems
The duo-gland adhesive system is one of the most widespread
mechanisms of temporary adhesion in benthic animals.
All echinoderm species possess such a system with two
types of NCS cells secreting an adhesive and ciliated
secretory (CS) cells enclosing small homogeneous electrondense granules and controlling de-adhesion (Flammang,
2006; Hermans, 1983). De-adhesion occurs at the outermost
fuzzy coat of the cuticle (Flammang, 1996). According to
one hypothesis, the de-adhesive function of the CS cells
is enzymatic, releasing the fuzzy coat from the underlying
cuticular layer [indeed, as Flammang (1996) reported, in
transmission electron micrographs of detached podia, the
fuzzy coat was no longer distinguishable] (see also Flammang,
Demeulenaere & Jangoux, 1994; Flammang et al., 1998,
2005) (Fig. 2D, E). After de-adhesion, the secreted adhesive
is left behind on the substratum as a footprint. Others
proposed that the role of CS cells is ‘‘neurosecretorylike’’, directly controlling or terminating the release of the
adhesive (Ball & Jangoux, 1990). According to this hypothesis
‘‘[considering that] the cuticle in some echinoderms may
act as an anti-fouling surface and will only function in
adhesion for so long as an adhesive secretion is being actively
secreted (McKenzie 1987) . . . there is no requirement for
a separate de-adhesive secretion’’ (Ball & Jangoux, 1990,
p. 208).
(b) Mono-gland systems
In a number of benthic animals, although adhesion is
controlled biochemically, de-adhesion is achieved without
the secretion of additional material. In the monogenean
(platyhelminth) parasite E. soleae, two different materials are
released to its host, and it was initially hypothesised that
the two secretions are products of a duo-gland adhesive
system (Tyler, 1988). However, Kearn & Evans-Gowing
(1998) showed that both secretions are adhesive, interacting
to form a glue, and that de-adhesion is most likely controlled
by enzymes found at the anterior adhesive area of the
integument.
Other animals control de-adhesion mechanically: The
monocotylidan monogeneans N. rhinobatidis and T. rhinobatidis possess apertures than open and close and duct endings
that evert during adhesion and retract during detachment.
In this way, the animal can pull itself away from the substratum mechanically (Whittington et al., 2004) (Fig. 2F, G).
Cuvierian tubules autotomise, leaving the sea cucumber
free to crawl away (see Section IV.2ci). The tentacles of
Nautilus pompilius detach by bending movements of their
musculature (Kier, 1987). Cyprids also control de-adhesion
without the secretion of additional material, although little is known about the detachment mechanism of these
larvae.
Flammang et al. (2005) investigated the variability of a
number of adhesives and found that, unlike permanent
adhesives, temporary adhesives of disparate benthic phyla
share common amino acids, indicating ‘‘convergence
in composition because of common function (i.e. nonpermanent attachment to the substratum) and selective
pressures’’ (p. 207). Adhesives of duo-gland systems are
similar to tissue adhesives, with relatively high amounts
of glycine, proline, isoleucine, and cysteine, whereas quick
adhesives form a distinct group with particularly high levels
of glycine (254–298 residues per thousand in the adhesives
of Cuvierian tubules of four holothurians vs. 97 residues
in Asterias rubens and 124 in E. solea) (Flammang, 2006;
Hamwood et al., 2002).
III. MICRO- AND MESOSCOPIC SURFACE
GEOMETRY AND MATERIAL PROPERTIES
The efficacy of an attachment depends on the quality
of the geometrical match between the adhesive organ
and the substratum. This match is enhanced at a microand mesoscopic level by: (a) material deformability, the
ability of the adhesive organs to match the complex and
unpredictable profile of the substratum, and (b) surface
structures, namely cilia, cuticular villi, papillae, and papulae.
Past studies primarily related these surface structures to
the presence of sensory and secretory cells lying in and
underneath the epidermis. Here we focus on the mechanical
contribution of these surface structures to adhesion. Material
deformability, cilia, and cuticular villi affect adhesion at
a microscale, and papillae and papulae contribute at a
mesoscale.
(1) Material deformability
Santos et al. (2005a) showed that sea urchins and sea stars
exhibit higher adhesion on rough than on soft substrata.
They also showed that this happens because the tube feet
deform in a viscoelastic manner to match the profile of the
substratum (Fig. 3A, B). Under slow self-imposed forces the
tube foot exhibits viscous behaviour to adapt to the roughness
of the substratum, whereas under short pulses of wavegenerated forces, the attached tube foot behaves elastically
to distribute the stress homogeneously along the area of
contact. The adhesive secretions fill only the small surface
irregularities in the nanometre range. This mechanism of
adhesion enhancement by material deformability resembles
the attachment mechanisms of grasshoppers (Gorb, Jiao &
Scherge, 2000) and tree frogs (Scholz et al., 2009) in terrestrial
environments, which deform their pads viscoelastically
to maximise contact with the substratum. Santos et al.
(2005a) were the first to report such behaviour in benthic
animals.
Biological Reviews (2010) 000–000 © 2010 The Authors. Journal compilation © 2010 Cambridge Philosophical Society
D. Dodou and others
8
A
D
B
C
E
F
Fig. 3. (A, B) Paired images showing viscoelastic deformations of the tube foot disc of the echinoid Paracentrotus lividus (right) to the
profile of the substratum (left): poly(methyl methacrylate) (A) and polypropylene (B) (Santos et al., 2005a). (C) Tuft of vibratile cilia
in the ctenophore Coeloplana bannworthi. VC: vibratile cilia (Eeckhaut et al., 1997). (D) Cuticular villi on the antennules of the cyprid
of the barnacle Balanus amphitrite (Phang et al., 2008). (E) Papillae on the buccal cones of the pteropod mollusc Clione limacina. Note
the projecting rosettes (arrows). c: motile cilia, p: papillae, sc: tufts of cilia (Hermans & Satterlie, 1992). (F) Papulae of the adhesive
knob in the sponge Tethya seychellensis (scale not reported in original). G: globiferous cells, P: papulae (Fishelson, 1981). The insets
correspond to the structural level illustrations in Fig. 1.
(2) Surface-projecting structures
(a) Cilia
Cilia are fine 5–10 μm long projections of cells and can
be non-motile or motile. Non-motile cilia act as sensory
organelles. Here we focus on motile cilia.
Motile cilia beat in a fluid (e.g. mucus) during locomotion,
propulsion, or food transfer. Motile cilia have been found in a
number of larvae, such as the barrel-shaped doliolaria larvae
of crinoids. These larvae are equipped with an attachment
complex of a ciliary cap with secretory cells, an apical tuft with
sensory cells, and an adhesive pit (Jangoux & Lahaye, 1990;
Nakano et al., 2003). Each of the sensory cells bears a long
cilium which is vibratile and beats in the mucus produced
by the secretory cells, while the tuft brushes the substratum.
The combined action of the secretory and sensory cells
allows the larva to move and explore the substratum while
remaining loosely attached to the water-substratum interface
(Flammang, 1996; Jangoux & Lahaye, 1990).
In the ctenophore Coeloplana bannworthi, an indirect role of
vibrating cilia in adhesion has been observed. This animal
has two tentacles with numerous tentilla. Six different types
of cells have been found on the tentilla surface, including
cells with 7-μm long cilia, cells with short pegs, and adhesive
cells (collocytes). According to Eeckhaut et al. (1997), the cilia
(Fig. 3C) are longer than the pegs, and therefore are the
first to be stimulated by vibrations caused by prey. This
activates the motion of the tentilla which contract and bring
the prey closer to the tentillum surface. As soon as the prey
touches the pegs at the tentillum surface, the pegs stimulate
the nearby collocytes via connecting nerves, the collocytes
elevate slightly, and the prey sticks to them.
(b) Cuticular villi
Cuticular villi are fine 1–2 μm long hairy structures on the
adhesive organs of cyprids and contribute to adhesion in a
unique way. Phang et al. (2008) observed cuticular villi at the
terminals of the antennules of the Balanus amphitrite cyprid
(Fig. 3D) and developed a number of hypotheses about the
role of villi in cyprid adhesion. According to one of these
hypotheses, the villi penetrate the adhesive and contact the
substratum directly in a similar manner to the spatulae
of geckos. The role of the secreted material is to displace
water to provide a local environment with a lower dielectric
constant than water, therefore increasing the interaction
forces between the villi and the substratum. If this hypothesis
is correct, cyprids are the only animals known to utilise a
combination of wet and dry attachment underwater (Phang
et al., 2008; see also Aldred & Clare, 2008).
(c) Papillae
The adhesive organs of benthic animals are generally covered
with adhesive papillae: protruding surface structures through
which adhesives are released. In the buccal cones of the
Biological Reviews (2010) 000–000 © 2010 The Authors. Journal compilation © 2010 Cambridge Philosophical Society
Mechanisms of temporary adhesion in benthic animals
mollusc Clione limacina Hermans & Satterlie (1992) observed
that, in addition to secreting adhesive material, papillae that
are 15 μm high and 10 μm in diameter also contribute to
adhesion mechanically. When the buccal cones are retracted,
the epidermis between clusters of papillae is folded, whereas
when the buccal cones are extended, the clusters stand proud
(Fig. 3E). These observations led Hermans & Satterlie (1992)
to conclude that food-capture mechanism of Clione limacina is
not only due to chemical adhesion; papillae enhance gripping
via mechanical interlocking.
The larval tentacles of the dendrochirote holothurian Aslia
lefevrei bear numerous approximately 200 μm long projecting
papillae that contribute mechanically to adhesion by increasing the area of contact (Costelloe, 1988). Keogh & Keegan
(2006) found that the tube feet of the ophiuroid Amphiura
filiformis are also covered with papillae, whereas the tube feet
of Amphiura chiajei are smooth, and they attributed this difference to the feeding styles of the two species: A. filiformis is a
suspension feeder and requires a large filtering area, achieved
by means of the sticky papillae. The smooth podia of A. chiajei,
on the other hand, are sufficient for deposit feeding.
(d) Papulae
A peculiar surface structure has been found on the
podial surface of two sponge species, Tethya seychellensis
and T. aurantium (see Section IV.2aii, for discussion on the
motile podia in sessile sponges). In a study on the transport
capabilities of these two sponges, Fishelson (1981) described
the presence of papulae with knobby ends. Although of
similar shape to the papillae described above, these papulae
were larger: approximately 90–100 μm long and 60–80 μm
wide (Fig. 3F). The papulae were visible before the initiation
of adhesion, but flattened and disappeared when the podia
came into contact with the substratum making the surface of
the adhesive knob smooth and possibly more adaptable to
the profile of the substratum.
A
1 cm
9
IV. MACROSCOPIC EXTERNAL MORPHOLOGY
We identified two types of macroscopic external morphology
relevant to properties of the structures that the animal
needs to adhere to: (a) low-curvature morphologies and (b)
projecting morphologies. In low-curvature morphologies,
adhesives are secreted along the mantle of the animal,
whereas in projecting morphologies, adhesives are secreted
from the extremities. We distinguished two groups of lowcurvature morphologies (extended and localised) and three
groups of projecting morphologies (multiple feet, branched
feet, and tentacular appendages).
(1) Low-curvature morphologies
(a) Extended low-curvature morphologies
For relatively demanding functions such as strong temporary
attachment in harsh habitats, benthic animals exhibit
extended low-curvature morphologies, in which adhesion
is activated and de-activated over a large area. Two cases of
such adhesive systems have been described in the literature:
the cephalopods Sepia spp. which use a combination of
adhesion and suction, and the cephalopod Euprymna scolopes
which uses temporary adhesion for camouflage.
Sepia spp. (Mollusca, Cephalopoda) live in wave- and
windswept rocky habitats with turbulent water flows and
require quick and very strong attachment. To achieve that,
at least three species of Sepia (S. tuberculata, S. typica, and
S. papillata) use a combination of suckers and adhesives
secreted along the ventral surface of the mantle of the
animal and the posterior surface of the ventral arms
(see Von Byern & Klepal, 2006, for a review) (Fig. 4A).
Behavioural studies for S. papillata are missing, but for S.
tuberculata and S. typica the mantle first contracts to create
a sucker-like cavity for quick attachment following which
an adhesive is released to reinforce the bonding with the
substratum. In S. tuberculata the adhesive area has ridges that
presumably enhance attachment (Roeleveld, 1972) (Fig. 4A).
B
Fig. 4. Low-curvature morphologies. (A) Ventral surface of the cephalopod Sepia tuberculata showing the adhesive area (black arrows)
on the mantle (Von Byern & Klepal, 2006). (B) Morphology of the mantle (white arrow) and fin (black arrow) of the cephalopod
Idiosepius biserialis (Von Byern & Klepal, 2006). The insets correspond to the structural level illustrations in Fig. 1.
Biological Reviews (2010) 000–000 © 2010 The Authors. Journal compilation © 2010 Cambridge Philosophical Society
D. Dodou and others
10
Histochemical analyses reviewed by Von Byern & Klepal
(2006) showed the presence of two kinds of glandular cell
that may both contribute to adhesion, but a comprehensive
understanding of this adhesive mechanism as well as the
mechanism that initiates suction is missing.
Euprymna scolopes uses an extended low-curvature adhesive
system for camouflage. This cephalopod burrows under sand
and cements sand grains to its body using adhesives secreted
from its dorsal epidermis (Moynihan, 1983a; Singley, 1982).
Shears (1988) observed that E. scolopes did not use a sand
coat at night but only when forced to emerge from the
sand during the day for feeding. The animals stayed at a
maximum distance of two body lengths from the substratum,
where camouflage would be most effective. Shears (1988) also
found that a sand coat inhibited the animal’s movements,
making prey capture more difficult and suggesting that the
camouflage functions as protection from predators rather
than in assisting prey capture. The sand coat also acts as a
defensive mechanism: when threatened, the animal releases
the sand instantaneously to distract the predator (Shears,
1988). Shears (1988) further suggested that the sand coat
may serve in sediment consolidation, preventing debris from
entering the mantle and allowing the animal to breathe when
buried in the sand; the use of the sand coat for camouflage
may have evolved from this initial function. The mechanism
causing rapid de-adhesion of such a large area (the entire
mantle) remains unexplored.
(b) Localised low-curvature morphologies
In flat water and stagnant environments the attachment
area does not need to be extended; the adhesive function
can be localised to a relatively small area of the epidermis.
For example the tiny cephalopod Idiosepius sp., at just a few
millimetres long, uses a small adhesive area in the posterior
region of its mantle and fins to temporarily attach to sea
grass or algae for camouflage (Moynihan, 1983b; Von Byern
et al., 2008) (Fig. 4B). The absence of musculature and nerve
A
B
fibres connected to the glandular cells of these regions rules
out the hypothesis that the animal uses suckers. Its adhesion
is probably achieved by means of a viscous mucous layer or
a duo-gland system as those described in Section II.3a.
(2) Projecting morphologies
(a) Multiple-feet projecting morphologies
Multiple-feet projecting morphologies consist of proximal
flexible stems endings in sensory/secretory/adhesive apices.
From the adhesive systems found in the literature, we
distinguished four main designs: tube feet, podia in sponges,
arms for free walking, and threads for restricted walking.
( i ) Tube feet. Tube feet occur in echinoderms as external
appendages of the water-vascular system and consist of
a proximal flexible and extensible stem ending in a distal
area that secretes adhesive material. Whereas the histological
structure of tube feet is similar for all echinoderms (consisting
of an inner mesothelium around the water-vascular lumen,
a connective tissue layer, a nerve plexus, and an outer
epidermis covered with a cuticle), a number of tube-foot
morphotypes exist: disc-ending, knob-ending, and penicillate
(reviewed by Flammang, 1996). Flammang (1996) discussed
three other types of tube feet as well: lamellate, ramified,
and digitate podia. Lamellate podia (knob-ending podia
with a flattened and folded stem) are respiratory and nonadhesive, and therefore not included here. Ramified (peltate
or pinnate) and digitate podia are discussed under branchedfeet projecting morphologies (Section IV.2b).
Disc-ending tube feet consist of a flexible stalk (the
stem) that ends in a flattened adhesive area (the disc)
(Fig. 5A). Function- and habitat-related variations in discending tube feet morphology have been observed. In
asteroids living in rocky intertidal areas, the disc is reinforced
with collagen fibres that enable stronger attachment than
simple disc-ending tube feet do (Santos et al., 2005b). In
echinoidea, disc-ending adoral tube feet usually have a
C
Fig. 5. Tube-foot morphotypes. All three consist of a stem ending in an adhesive disc of various forms (arrows). D: disc, S: stem.
(A) Simple disc-ending tube foot of the echinoid Heterocentrotus trigonarius (Santos et al., 2009). (B) Knob-ending tube foot of the asteroid
Astropecten irregularis (Santos et al., 2009). (C) Penicillate tube foot of the echinoid Echinocardium cordatum (Flammang, 1996). The insets
correspond to the structural level illustrations in Fig. 1.
Biological Reviews (2010) 000–000 © 2010 The Authors. Journal compilation © 2010 Cambridge Philosophical Society
Mechanisms of temporary adhesion in benthic animals
thicker, stronger, and more extensible stem, and an enlarged
disc as compared to aboral feet (Flammang & Jangoux,
1993; Leddy & Johnson, 2000; Santos & Flammang, 2005;
Smith, 1978). This differentiation is possibly function-related
(Flammang & Jangoux, 1993): Adoral tube feet are used
in locomotion and anchorage, whereas aboral tube feet
function in postural changes and food capture. The tube foot
diameter, number, thickness, density, and development also
vary with functional requirements. Unlike the suggestion of
Smith (1978), larger animals do not necessarily possess a
larger number of tube feet. Increased adhesion can result
from the combined effects of variables such as tube foot
number and arrangement, mechanical properties, etc. (see
Santos & Flammang, 2005). Disc-ending tube feet have also
been found in holothuroids (Flammang & Jangoux, 1992)
and sand dollars (Clypeasteroida) (Mooi, 1986a, b; Nichols,
1959; Telford & Mooi, 1986; Telford, Mooi & Harold, 1987).
Knob-ending tube feet consist of a stem ending in a
pointed knob (Fig. 5B). Within the asteroids, Paxillosida
are the only order possessing adhesive knob-ending tube
feet (Santos et al., 2005b; Vickery & McClintock, 2000).
Paxillosida bury themselves completely within the sediment
and use their adhesive tube feet for locomotion as well as for
sand burrowing. Vickery & McClintock (2000) reported
a variation on knob-ending tube feet in the paxillosid
Macroptychaster accrescens which has slightly rounded tips.
The exact adaptive value of knob-ending tube feet remains
unclear.
Irregular echinoids of the order Spatangoida possess
penicillate tube feet (Flammang, 1996). These are similar
to simple disc-ending tube feet, but their adhesive disc has
numerous digitations, covering either the entire disc or only
its margin (Fig. 5C). Spatangoids live in burrows in the
sediment and use their tube feet for various functions: Those
located close to the mouth are used for collecting particles
from the floor of the burrow and for transporting them
to the mouth; those that are located in the posterior and
dorsal regions build and maintain the burrow (Flammang,
De Ridder & Jangoux, 1990; Nichols, 1959).
( ii ) Podia in sponges. Sponges are traditionally considered
as sessile metazoans. Fishelson (1981), however, observed
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11
that individuals of two sponge species, Tethya seychellensis and
T. aurantium, have podia consisting of a 10–16 mm long
and 0.3–1.0 mm wide flexible stem with a swollen, adhesive
knob at the distal end (Fig. 6A). Dormant while the sponge
remains undisturbed, these podia are activated when the
animal is covered by sediment, where upon they extend their
stem, sticking the knob at a distance from the sponge. The
knob becomes flattened as it adheres to the substratum and
the papulae on its surface disappear (see Section III.2d). The
podia then shorten and pull the entire sponge along via a
lever action. By this method the sponge can be moved to a
new site.
Although the external morphology of these podia has
similarities with the tube feet of echinoderms (proximal
stem, distal adhesive end), their internal morphology is
completely different. Sponge podia lack the water-vascular
system that characterises echinoderm tube feet; instead, they
have a gelatinous core containing bundles of microfibers and
myocytes, primary archaeocytes, nucleated archaeocytes,
and scleroblastic cells, all of which contribute to the mobility
of the sponge podia. The myocytes are contractile and are
partially responsible for the shortening of the podia, whereas
the nucleated archaeocytes undergo a process of ripening
to produce collagenic filaments deposited in the adhesive
matrix. The gelatinous core is surrounded by a layer of
globiferous (excretory) cells (see Fig. 3F); these are bottleshaped with their neck reaching on the sponge surface and
responsible for releasing adhesives. Sponge podia are capable
of directional movement, similar to that of sea urchin tube
feet, but at much slower time scales.
( iii ) Arms for free walking. In the last pre-metamorphic
phase, during which the larvae search for a suitable site
to settle for metamorphosis, larvae have mechanisms to
prevent being swept away by water currents (e.g. Butman,
Grassle & Webb, 1988; Mullineaux & Butman, 1991; Pawlik,
Butman & Starczak, 1991). The brachiolaria larvae of sea
stars are equipped with three arms and an adhesive disc
(Haesaerts et al., 2005a; Haesaerts, Jangoux & Flammang,
2005b). Each arm consists of a stem ending in a distal
adhesive crown (Fig. 6B). The brachiolaria larva explores
the environment, and when it detects a suitable substratum
B
C
Fig. 6. Multiple-feet projecting morphologies. (A) The sponge Tethya seychellensis with some of the extended podia free and other
adhered [scale is not given in the original, but Fishelson (1981) reported that the podia are 10–16 mm long, for sponges 2–3 cm in
diameter]. AP: adhered podia, FP: free podia (Fishelson, 1981). (B) Arm of a brachiolaria larva of the sea star Asterias rubens. The
arm consists of a stem and ends in an adhesive apex. AP: adhesive apex, S: stem (Haesaerts et al., 2005b). (C) Cyprid of the barnacle
Balanus amphitrite with adhesive antennules (arrow) (Phang et al., 2008). The insets correspond to the structural level illustrations in
Fig. 1.
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D. Dodou and others
12
for metamorphosis, it directs two or three arms towards the
site, secretes an adhesive, and attaches temporarily. Then
it alternatively attaches and detaches each brachiolar arm
and ‘‘walks’’ along the substratum. The brachiolar arms
are morphologically similar to the tube feet of the adult
sea star: they both consist of a proximal flexible stem and
a distal sensory-secretory area (Haesaerts et al., 2005a, b).
These morphological similarities (as well as the similarities
in the biochemical content of the adhesive systems described
in Section II) between brachiolaria larvae and adult sea stars
possibly reflect an economy at the genetic level (Haesaerts
et al., 2005b).
Turbulent channel flow measurements showed that shear
stresses of about 1 Pa can dislodge temporarily attached
brachiolar arms. This value is surprisingly low compared
to typical stresses in a wave-swept environment, which can
reach up to 10 Pa. However, the value of the shear stress in
the channel flow does not correspond to field conditions
because the applied water channel creates a turbulent
boundary layer with a steady overall flow rate, whereas in the
field high shear stresses last only few seconds and the forces
applied on the larvae are reduced due to the roughness of the
substratum and the neighbouring organisms (Haesaerts et al.,
2005a). Organisms can be more easily dislodged by lasting
steady shear stresses than by the high but brief peaks, which
can explain why brachiolar larvae seem to sustain much
higher shear stresses in the field than in the water channel.
( iv ) Threads for restricted walking.
During the premetamorphic stage, some larvae adopt a strategy of restricted
walking: they stick to the substratum by means of flexible
threads, so that they can move and explore whether the
surface is suitable for settlement, while remaining loosely
attached to it. In contrast to the other surface structures
described here, threads are extracellular. Cyphonautes,
a larval form of the bryozoan Membranipora membranacea,
for example, secrete mucus threads during exploration,
A
which attach to the substratum, while the larva keeps
moving around (Atkins, 1955); the exact adhesive mechanism
remains unknown. It is interesting that cyphonautes explore
habitats in all directions and often upstream (Abelson, 1997).
This is a rather unusual property considering that larvae
mostly tend to settle in areas of low hydrodynamic stress,
where they are less likely to be washed away (e.g. Abelson,
1997; Abelson & Denny, 1997; Koehl & Hadfield, 2004; see
also Koehl, 2007, for a review).
A similar mechanism of attachment was studied by
Abelson, Weihs & Loya (1994) in coral larvae, which produce
mucous threads up to 100 body lengths in size and are able
to settle in environments of high food-particle fluxes and low
sedimentation rates. Other larvae using threads include the
doliolaria larvae of crinoids, described in Section III.2a, and
the cyprid larvae of barnacles (Fig. 6C), described in Section
III.2b.
(b) Branched-feet projecting morphologies
Branched-feet projecting morphologies consist of a main
flexible trunk with side and terminal branches; the
apices of the terminal branches have one or more
sensory/secretory/adhesive apices. Often located around
the mouth, most branched-feet projecting morphologies
are passively exposed to the water and used for funnel
and suspension feeding. Here we focus on branched-feet
projecting morphologies used in functions requiring stronger
adhesion than funnel or suspension feeding. Three types of
such podia are relevant: digitate, peltate, and pinnate.
( i ) Digitate podia. Digitate podia are cylindrical with
a slender tip (Fig. 7A). They occur in ophiuroids and
crinoids, and due to their histological similarities to tube feet,
Flammang (1996) classified them as tube-foot morphotypes.
In their studies on the crinoid Antedon bifida, Nichols (1960)
and Lahaye & Jangoux (1985) also characterised digitate
podia as tube feet. The shape of digitate podia is similar
B
C
1 mm
Fig. 7. Branched-feet projecting morphologies. (A) Digitate podia of the ophiuroid Ophiothrix fragilis (Santos et al., 2009). (B) Peltate
buccal tentacle of the aspidochirotid holothurian Paroriza prouhoi. c: ciliates, d: digits (Roberts & Moore, 1997). (C) Pinnate tentacles
in the holothurian Synapta maculata P: pinnule, S: stem (Flammang & Conand, 2004). The insets correspond to the structural level
illustrations in Fig. 1.
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Mechanisms of temporary adhesion in benthic animals
to the knob-ending podia described in Section IV.2ai, but
digitate podia are smaller (see Figs 5B, 7A) and belong to a
branched morphology. Digitate podia are mostly involved
in catching particles and filter feeding (Pentreath, 1970;
Warner, 1982), functions which may explain why adhesive
papillae are discretely distributed, whereas in disc-ending
and knob-ending tube feet the adhesive area is large and
continuous, allowing strong attachment for locomotion or
for maintaining position (Santos et al., 2009).
( ii ) Peltate and pelto-digitate tentacles.
Peltate tentacles
occur in aspidochirotid holothurians and elasipods, which
are both deposit feeders. The basic shape of these tentacles
is cauliflower-like (Fig. 7B), but a large number of functionrelated variations exist (Hudson et al., 2003). The elasipod
Laetmogone violacea, for example, has peltate podia with a
large adhesive surface area that enables sweeping off the
sediment. The aspidochirotid Bathyplotes natans, on the other
hand, has finer peltate-like tentacles, with a higher degree
of branching that enables the selection of high-quality
detrital particles without taking up much sediment. The large
aspidochirotid Paroriza pallens is equipped with tentacles that
are intermediate between peltate and digitate (pelto-digitate;
Roberts & Moore, 1997). Pelto-digitate tentacles allow the
animal to plough the seabed ingesting large quantities of
sediment (Hudson et al., 2003). Other elasipodid as well
as aspidochirotid holothurians with peltate or pelto-digitate
tentacles are described in Roberts & Moore (1997).
( iii ) Pinnate tentacles. Although apodid holothurians are
deposit feeders, they are not equipped with peltate tentacles,
but with pinnate tentacles. Roberts (1982) argued that
pinnate tentacles are more efficient than peltate tentacles. An
apodous holothuroid with pinnate podia is Synapta maculata,
a holothuroid that reaches lengths of 5 m – considerably
larger than other holothurians which have a typical length of
20 cm, the smallest are less than 1 cm. The pinnate tentacles
of Synapta maculata are more prehensile than those of other
apodid holothurians, enabling them to wrap sea grass leaves
or press against soft surfaces (Flammang & Conand, 2004)
(Fig. 7C). The external epidermis of the tentacles contains
a duo-gland system with adhesive secretions employed for
collecting and handling particles and de-adhesive secretions
facilitating the release of the particles into the mouth.
(c) Tentacular projecting morphologies
For capturing a moving target (prey or a mate) or
immobilizing a predator, benthic animals use tentacles that
first mechanically immobilise the target and then release an
adhesive to create an attachment. The mechanisms can
be divided into two groups: autotomising tentacles and
retracting tentacles. The former are used to immobilise a
predator and then autotomise, allowing the intended prey to
crawl away. The latter are employed for feeding and mating
and are pulled back into the animal’s body after use.
( i ) Autotomising tentacles. The most well-known mechanism of autotomising tentacles is that of Cuvierian tubules
(Figs. 2C, 8A). Apart from the unique character of the
secreted adhesive described in Section II.2b, the adhesive
13
strength of Cuvierian tubules depends on the morphological and mechanical properties of their inner tissues. For
example, Flammang et al. (2002) found up to three times
higher tenacities for shear loadings compared to peeling and
suggested that the difference in tenacity for both directions
can be related to function: ‘‘The higher tenacities associated with shear loading and preliminary compression of the
tubules indicate that Cuvierian tubules are well tailored for
functioning as adhesive defense organs. Indeed, in nature, a
potential predator entangled in Cuvierian tubules will most
likely apply shear loads on the tubules and will therefore
experience high adhesion strengths. Moreover, by pulling on
the tubules when trying to free itself, it will also maximize
their stickiness.’’ (Flammang et al., 2002, p. 1114).
( ii ) Retracting tentacles. Tentacular projecting morphologies can also be used for capturing prey or mates. The
tentacles are retracted into the animal’s body after use, but
their structure and mechanisms strongly resemble that of
autotomising tentacles.
Retracting tentacles have been found in the cephalopod
Nautilus sp. Cephalopods usually use suckers for attachment
but a few families of this class use adhesive secretions
instead (see Von Byern & Klepal, 2006, for a review).
Nautilus sp. has numerous tentacles without suckers or arm
hooks to attach to a substratum, capture prey, or cling
to other individuals during mating. Instead, the tentacles
secrete adhesive granules that contain carbohydrates and
proteins (Barber & Wright, 1969; Kier, 1987; Muntz &
Wentworth, 1995).
Clione limacina (a pteropod mollusc) possesses a faststrike feeding tentacular apparatus (studied by Hermans
& Satterlie, 1992), which resembles the tentacles of Nautilus
sp. In the presence of a prey item, the mollusc opens its
mouth within 10–20 ms; then, in 50–70 ms, three pairs
of oral appendages, called buccal cones, are hydrostatically
inflated, extruded, surround the prey, and release a viscous
material that adheres to the shell of the prey (Fig. 8B).
A third mechanism of retracting tentacles is that of Coeloplana
bannworthi (Ctenophora, Platyctenida), described in Sections
II.2b and III.2a.
V. DISCUSSION
We reviewed the temporary adhesion of benthic animals
from the perspective of three structural levels: the
biochemical content of the adhesive secretions, the microand mesoscopic surface geometry and material properties,
and the macroscopic external morphology of the adhesive
organs. We classified the temporary adhesive systems of a
range of diverse animals into subcategories of these three
structural levels as described in Fig. 1, demonstrating that a
limited set of concepts holds for a wide range of temporary
adhesive systems, perhaps indicating convergent evolution.
In all reviewed cases, the adhesive secretions provide
binding to the substratum at a molecular scale, whereas
the surface and material characteristics and the external
Biological Reviews (2010) 000–000 © 2010 The Authors. Journal compilation © 2010 Cambridge Philosophical Society
D. Dodou and others
14
A
B
Fig. 8. Tentacular projecting morphologies. (A) The holothuroid Bohadschia argus with Cuvierian tubules in view (courtesy
P. Flammang). (B) The pteropod mollusc Clione limacina with mouth open and five of the six buccal cones protruded. bc: buccal
cones, m: mouth, t: tentacles (Hermans & Satterlie, 1992). The insets correspond to the structural level illustrations in Fig. 1.
morphology increase the contact area with the substratum
from micro- to macroscales. From a cost-effectiveness pointof-view, a minimal amount of adhesive should be secreted,
particularly for common activities such as locomotion and
feeding. This can be achieved by means of strongly adhesive
molecules, but also by the adaptability of a surface. It is
also possible that a trade-off exists between the softness of the
material which the adhesive organ is made of and the amount
of the secreted adhesive, because an excessively soft material
would not be functional either. This trade-off may be further
dependent on the action for which adhesion is used. For
infrequent actions that are critical for the animal’s survival,
such as predator immobilisation, surface optimisation might
be less critical and larger amounts of adhesives must be used.
This could be why we found more refined and elaborate
surface structures and adaptive morphologies for common
functions such as feeding activities than for occasional ones
such as predator defence.
(1) Biological research
Using our perspective of the three structural levels, key areas
deserving further investigation can be identified.
There is mixed information on the performance of
adhesive secretions on substrata of different polarity.
Hennebert et al. (2008) reported that the footprints left by the
sea star Asterias rubens on glass, mica, and Teflon had identical
morphology, shape, and diameter, and that only the quantity
of the secreted adhesive was larger for hydrophilic than for
hydrophobic surfaces. Santos & Flammang (2006), on the
other hand, found similar tenacities of Paracentrotus lividus
on glass, polypropylene, and polystyrene, but higher values
on poly(methyl metacrylate). Moreover, ‘‘abiotic’’ surfaces
are usually covered with algal, microbial, or bacterial films
and the effect of these organic films on adhesion is not
known. A number of studies suggested that organic films
enhance larval settlement (e.g. Brancato & Woollacott, 1982;
O’Connor & Richardson, 1998), whereas others questioned
such facilitation (e.g. Keough & Raimondi, 1995; Roberts
et al., 1991). A more systematic investigation of adhesives
suitable for abiotic substrata may show whether these also
fulfil the requirements for adhesion to biotic substrata.
At the level of micro- and mesoscopic surface geometry
and material properties, it is possible that cilia contribute
mechanically to adhesion by increasing the contact area.
The contribution of cuticular villi to the adhesion of
cyprids by penetrating through the secreted adhesive to
provide direct contact with the substratum deserves further
investigation, considering that this may represent an unusual
combination of wet and dry adhesion underwater. Moreover,
it is possible that, due to their softness, papillae can adapt to
the irregularities of a surface, increasing the area of contact
and therefore the adhesive capability of the animal.
Turning to the level of macroscopic external morphology,
stem-disc structures are of particular interest in advancing
our understanding of how the shape of an adhesive
organ contributes to adhesion. Despite the apparent
differences between various tube-foot morphotypes and their
possible relations to function and habitat, no quantitative
comparisons have been made of the adhesive strength of these
different morphotypes. According to Santos & Flammang
(2005), the disc is important because it releases an adhesive,
whereas connective tissue in the stem withstands the tensions
exerted by the hydrodynamic forces. Gorb & Varenberg
(2007) suggested that a stem-disc morphology is a highly
favourable shape for adhesion. They manufactured model
stem-disc geometries and found that they can sustain up to
eight times larger pull-off forces than flat pillars can. They
also showed that there was a critical difference in the failure
mode of flat pillars and of stem-disc geometries during the
pulling: whereas in flat pillars contact separation started at an
arbitrary point at the disc edge and propagated through the
centre to the opposite edge as a straight line, during pulling
of stem-disc geometries a void was created in the centre of
the disc and developed towards the disc edges. The stronger
adhesion was due to the formation of this suction-like device
when pulling the flexible stem.
Quantitative data are lacking regarding low-curvature
morphologies: one might expect that due to their relatively
large size and ability to match the profile of a rough
Biological Reviews (2010) 000–000 © 2010 The Authors. Journal compilation © 2010 Cambridge Philosophical Society
Mechanisms of temporary adhesion in benthic animals
surface, low-curvature morphologies should be smoother
than projecting morphologies. In Fig. 4A, it is clear, however,
that the low-curvature ventral surface of Sepia tuberculata
consists of ridges at a microscale. A pattern of microscale
grooves can be also distinguished in Idiosepius sp. (Fig. 4B).
This micropattern in Idiosepius sp. reminds the recently
discovered nanopattern on the apparent flat (i.e. lowcurvature) tree frog toe pads (Scholz et al., 2009).
Future studies could investigate the movements accompanying the attachment and detachment of benthic animals.
Even for tube feet, which are considered passive attachment devices, the activation of muscles and/or direction of
macroscopic movements may be critical for adhesion and
de-adhesion.
Finally, little is known about the cost of adhesion in benthic
animals. Donovan & Carefoot (1997) estimated the energy
cost of adhesive crawling for the abalone Haliotis kamtschatkana
(transitory adhesion) and VandenSpiegel et al. (2000)
evaluated the efficiency of the regeneration mechanism of
Cuvierian tubules in the sea cucumber Holothuria forskali. By
investigating the cost of temporary adhesion mechanisms in
benthic animals, we can gain a better understanding about
the trade-offs involved.
(2) Comparative studies
Multivariate statistics may be used to test our categorisation
of adhesion mechanisms. Multivariate statistics have proven
of great use in comparative biology (Felsenstein, 1985),
particularly when morphological data are involved (Adams,
Rohlf & Slice, 2004; Koehl, 1996). Zani (2000) statistically
analysed independent contrasts of claw and toe morphology
and of clinging performance from 85 lizard taxa and found
that increased claw curvature, toe width, and number
of adhesive lamellae correlated with increased clinging
performance on smooth substrata, whereas increased claw
height and decreased toe length correlated with increased
clinging performance on rough substrata. Other studies have
investigated correlations between an animal’s morphology
and habitat (Irschick et al., 2005; Melville & Swain,
2000), or changes in morphology due to evolutionary
changes of function (Schulte et al., 2004; Verwaijen & Van
Damme, 2007). Statistical analyses should be combined with
quantitative mechanistic analyses (Koehl, 1996) in order to
understand how function depends on and affects adhesion
mechanisms at the three structural levels.
In this review, a number of adhesive systems were discussed
in more than one section, indicating that their adhesion
functions simultaneously at more than one structural level.
Therefore, we propose measuring and modelling adhesion
forces across scales, from molecular to macroscopic. In
geckos extensive studies revealed that multiscale hierarchical
(surface) structures allow these animals to grip substrata of
various roughnesses (Gao et al., 2004). It is likely that the
adhesion of benthic animals is also the result of multiscale
effects: surface viscoelasticity and structures initiate the points
of contact with the substratum at a micro- and mesoscale, the
adhesive secretions fill in surface irregularities at a nanoscale,
15
and external morphology provides support and/or increases
contact with the substratum at a macroscale. A selfevident but fundamental difference between the adhesive
mechanisms of terrestrial animals, such as geckos, and
of benthic animals is that the latter must displace water
to initiate contact with a surface. It is unknown whether
water displacement occurs due to the surface properties of
an adhesive organ (e.g. hydrophobicity/hydrophilicity), the
nature of their secretions, or results directly from jettison
action of the animal’s musculature.
Little is known about the operating time scales of
temporary adhesives compared to other modes of temporary
adhesion such as suction or dry adhesion. Some benthic
animals such as Sepia spp. (see Section IV.1a) use suction
as an initial phase of attachment and secrete temporary
adhesives afterwards to secure fixation to the substratum.
Limpets also use suction for short-term attachment (up to a
few hours) and switch to glue-like adhesion when they have
to remain attached for longer periods (Smith, 1991, 1992).
The tentacles of octopods and decapods only bear suckers
and do not produce adhesives; still the fast-swimming, openwater decapods of the suborder Oegopsida are able to
produce pressure differentials up to 800 kPa (Kier & Smith,
2002). The tentacles of Nautilus spp., on the other hand, lack
suckers and operate by means of adhesive secretions only.
A comparative study of sucker-based, secretion-based, and
dry attachment mechanisms and their operating time scales
may reveal the conditions in which each of these mechanisms
is most effective.
(3) Biomimetic potential
The environment of benthic animals has similarities to
the internal environment of mammals. Inside the human
body, tissues and organs are covered or surrounded by
fluids that resemble sea water with respect to pH and
ionic composition (Flammang et al., 2005). Consequently,
the temporary adhesion mechanisms of benthic animals
have become a source of inspiration for the development
of artificial biomedical adhesives (Albala, 2003; Lee et al.,
2007; Ninan et al., 2003; Strausberg & Link, 1990; Tatehata
et al., 2001).
Studies of geometry and morphology in terrestrial animals
have inspired the development of artificial dry adhesive
systems (Arzt, 2006; Crosby, Hageman & Duncan, 2005;
Geim et al., 2003; Gorb et al., 2007; Gravish et al., 2010; Sitti
& Fearing, 2003; Yurdumakan et al., 2005), whereas artificial
adhesive systems inspired by the adhesion mechanisms of
benthic animals have mainly been restricted to analysing
and mimicking the biochemical content of such systems
(Burzio et al., 1997; Deming, 1999; Taylor & Weir, 2000;
see also Flammang et al., 2005, for a review). Clearly,
optimisation of the chemical content of an adhesive is
important, but developers of artificial adhesive systems for
biomedical applications should also consider whether they
can improve adhesion in other ways. For example, whether
flexible and extensible bonds between two adhering surfaces
increase adhesion, whether an adhesive could be patterned,
Biological Reviews (2010) 000–000 © 2010 The Authors. Journal compilation © 2010 Cambridge Philosophical Society
D. Dodou and others
16
or whether multiple isolated adhesive regions are better than
an extended adhesive surface.
To obtain insight into the combined effects of morphology,
geometry, and secretions in biomedical adhesive systems,
Dodou, Del Campo & Arzt (2007) carried out a series of
in vitro experiments. Previous research (Dodou, Breedveld
& Wieringa, 2006) showed that adhesion to soft tissues
inside the human body can be considerably increased by
using mucoadhesives, which can be incorporated into the
feet of an in vivo robot that walks along the surface of soft
tissues or inside hollow organs. Dodou et al. (2007) showed
that a patterned adhesive generated significantly higher grip
as compared to non-patterned adhesive films. Non-adhesive
patterns yielded much lower friction values, in fact lower than
the friction generated by non-adhesive flat surfaces. These
findings corroborate that adhesion in wet environments can
be the combined result of mechanisms across scales, from
molecular to macroscopic.
VI. CONCLUSIONS
(1) Temporary adhesion in benthic animals can be
considered as a multiscale architectural problem of
molecular bonds in combination with an adaptive
geometric match between the adhesive organ and the
substratum from micro- to macroscopic levels.
(2) Disparate taxa share common adhesion mechanisms,
perhaps indicating convergent evolution.
(3) Optimisation of the chemical content of an adhesive is
important, but developers of artificial adhesive systems
should also consider that adhesion can be improved
in other ways, namely by optimising the contact area
through adaptive geometries.
VII. ACKNOWLEDGEMENTS
The research of D. Dodou is supported by the Dutch
Technology Foundation STW, Applied Science Division
of NWO and the Technology Program of the Ministry of
Economic Affairs. We thank two anonymous reviewers for
providing many constructive comments which helped to
improve this paper considerably. We also thank the Assistant
Editor for valuable amendments in the manuscript.
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