Fastest predators in the plant kingdom: functional morphology and biomechanics of suction traps found in the largest genus of carnivorous plants
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Fastest predators in the plant kingdom: functional morphology and biomechanics of suction traps found in the largest genus of carnivorous plants
Simon Poppinga 1 2
Carmen Weisskopf 0 2
Anna Sophia Westermeier 2
Tom Masselter 2
Thomas Speck 1 2
Associate Editor: James F. Cahill
0 Present address: Department of Biomaterials, Max Planck Institute of Colloids and Interfaces , Wissenschaftspark Potsdam-Golm, Am Mu ̈ hlenberg 1, 14476 Potsdam , Germany
1 Freiburg Materials Research Center (FMF), University of Freiburg , Stefan-Meier-Straße 21, 79104 Freiburg im Breisgau , Germany
2 Plant Biomechanics Group, University of Freiburg , Botanic Garden, Scha ̈ nzlestrasse 1, 79104 Freiburg im Breisgau , Germany
Understanding the physics of plant movements, which describe the interplay between plant architecture, movement speed and actuation principles, is essential for the comprehension of important processes like plant morphogenesis. Recent investigations especially on rapid plant movements at the interface of biology, physics and engineering sciences highlight how such fast motions can be achieved without the presence of muscles, nerves and technical hinge analogies. The suction traps (bladders) of carnivorous bladderworts (Utricularia spp., Lentibulariaceae, Lamiales) are considered as some of the most elaborate moving structures in the plant kingdom. A complex interplay of morphological and physiological adaptations allows the traps to pump water out of their body and to store elastic energy in the deformed bladder walls. Mechanical stimulation by prey entails opening of the otherwise watertight trapdoor, followed by trap wall relaxation, sucking in of water and prey, and consecutive trapdoor closure. Suction can also occur spontaneously in non-stimulated traps. We review the current state of knowledge about the suction trap mechanism with a focus on architectonically homogeneous traps of aquatic bladderwort species from section Utricularia (the so-called 'Utricularia vulgaris trap type'). The functional morphology and biomechanics of the traps are described in detail. We discuss open questions and propose promising aspects for future studies on these sophisticated ultra-fast trapping devices.
Biomechanics; bladderwort; carnivorous plant; functional morphology; prey; suction trap; Utricularia
Carnivorous plants attract, catch, retain and kill prey
animals and absorb the nutrients resulting from digestion
(Darwin 1875; Lloyd 1942)
. This ‘carnivorous syndrome’
has evolved several times independently in angiosperms
and can be regarded as an adaptation to a life in
(Juniper et al. 1989; Albert et al. 1992;
Barthlott et al. 2007)
. Carnivorous plants are termed
‘active’ when their traps perform motion, as, for example,
the slow movements of Drosera (sundew) leaf blades to
retain prey. Apart from the classical textbook division into
taxes, tropisms, nastic and autonomous motions, such
plant movements can also be described according to
their actuation principle. Hydraulic motions function due
to a displacement of water between cells and tissues,
which can be active (turgor changes in living cells) or
passive (swelling/shrinking processes of dead cells,
cohesionforce driven motion). The speed of hydraulic movement
primarily depends on the dimension (thickness) of the
respective plant organ which the water has to flow through
and, hence, is ultimately limited by the speed of this
process of water diffusion
(Skotheim and Mahadevan 2005)
Some active carnivorous plants have evolved traps that
can move faster as theoretically possible due to pure
(reviewed by Forterre 2013; Poppinga et al.
. A well-known example for this phenomenon is
the snap-trap of the Venus flytrap (Dionaea muscipula,
Droseraceae), which performs a combination of
stimulustriggered, active hydraulic motion followed by a passive
release of elastic energy stored in the trap lobes
(Forterre et al. 2005)
. Such elastic components
greatly boost the overall speed of the motion, which
otherwise would be too slow for the carnivorous plant
to overcome prey. The understanding of such mechanical
‘tricks’ not only leads to a deepened understanding of the
ecology and evolution of a plant and its trapping
(Gibson and Waller 2009; Poppinga et al. 2013b)
can also give great inspiration for implementation into
bio-inspired technical materials
(reviewed by Guo et al.
The recent proof of carnivory in Philcoxia with
belowground sticky traps
(Pereira et al. 2012)
, the discovery of
ancient sticky trap fragments in Eocene Baltic amber
(Sadowski et al. 2015)
and comprehensive analyses of
passive-dynamic prey capture mechanisms
(Bauer et al.
demonstrate that carnivorous plants are always
good for ‘a surprise’. In this review, we summarize the
current state of knowledge about the fastest active
trapping mechanism known, the suction trap, which is far
from being completely understood. We believe that it
also holds ready ‘scientific surprises’ and hope to inspire
future research on these still enigmatic and mechanically
highly complex devices.
Carnivory in the Lentibulariaceae
Within the flowering plant family Lentibulariaceae (order
Lamiales), three carnivorous genera with different prey
capture mechanisms exist. Genlisea (corkscrew plants)
feature sub-terrestrial eel-traps
(Darwin 1875; Lloyd
1942; Fleischmann 2012a)
, Pinguicula (butterworts)
develop active sticky leaves
(Darwin 1875; Lloyd 1942;
and Utricularia (bladderworts)
capture and digest small prey animals with active suction
(Darwin 1875; Treat 1875; Lloyd 1942; reviewed by
Guisande et al. 2007)
. The family name can be deduced
from the Latin word for ‘lentil’ (lens), referring to the
lentiform traps of Utricularia, whereas the bladderwort’s
genus name can be ascribed to the term ‘utriculus’,
which refers to the shape of a wineskin.
Bladderworts constitute the largest genus of
carnivorous plants and comprise 240 species
Fleischmann 2012b, 2015)
. Molecular phylogenetic
reconstructions showed that Pinguicula holds a basal
position in the Lentibulariaceae and that Genlisea and
Utricularia are more derived sister genera
(Mu¨ ller et al.
2000, 2004, 2006; M u¨ller and Borsch 2005; Fleischmann
. The aquatic U. gibba possesses one of the
smallest angiosperm genomes so far known (only rivalled
by some species of Genlisea)
(Greilhuber et al. 2006;
Fleischmann et al. 2014; Veleba et al. 2014)
, which is
furthermore characterized by only a tiny portion of
noncoding DNA (Ibarra-Laclette et al. 2013).
classified 35 sections within Utricularia according to
morphological traits, including trap shape, position of trap
entrance and door, and position and shape of trap
appendages. The molecular systematic analyses by
Jobson et al.
, M u¨ller et al. (2004) and M u¨ller and Borsch (2005)
generally corroborate this classification, and the three
subgenera Polypompholyx, Utricularia and Bivalvaria
have been proposed
(Mu¨ ller et al. 2006)
. The sections
Utricularia and Vesiculina (U. subgen. Utricularia)
comprise nearly all aquatic bladderworts, and the 35 species
in section Utricularia share a common trap architecture
(the ‘Utricularia vulgaris trap type’)
(Lloyd 1935, 1942;
that will be described in detail with all its
structural and functional variations in this article.
Biophysical investigations on Utricularia have been conducted for
the most part on this trap type, as the respective aquatic
species possess relative large traps and are comparably
easy to access and cultivate.
Distribution and Life-forms of Utricularia
Utricularia can be found almost worldwide, with hotspots
of diversity in South America and Australia
Bladderworts occur rarely in arid regions as they need at
least seasonal humidity to thrive. The widest distribution
is shown by some aquatic or semi-aquatic species that
can be found in the entire circumboreal region
1942; Taylor 1989; Barthlott et al. 2007)
Bladderworts grow in diverse habitats, all being
characterized by soils or water poor in nutrients and sparse
competition. According to their habitat, species can be divided
into several life-forms, whereas the boundaries between
these life-forms are often vague and intermediate forms
(Brewer-Carias 1973; Van Steenis 1981; Taylor 1989;
M u¨ller and Borsch 2005; Reifenrath et al. 2006; Barthlott
et al. 2007)
. Terrestrial species grow on wet soils, e.g. in
constantly wet peat or in sand savannah communities
where seasonally no surface water is visible. The soil
has to be wet at least in the growth periods of the plants,
but waterlogged soils are preferred by most species. If
growing on banks, the plants can become temporarily
submersed but remain anchored to the ground. This
group contains more than half of all known Utricularia
species (e.g. U. prehensilis, U. trichophylla and U. uliginosa).
Facultative epiphytic (e.g. U. alpina) and facultative
lithophytic species (e.g. U. sandersonii) can be found growing,
for example, on tree trunks or on wet rocks, respectively.
Aquatic species grow in more or less oligotrophic waters,
either free-floating (e.g. U. vulgaris) or anchored
submersed (e.g. U. intermedia). In the latter case, the plants
are affixed to the ground with modified root-like shoots
or make use of specialized anchoring devices for a life in
vastly streaming water (rheophytes) (e.g. U. rigida). The
classification of anchored submersed species as aquatic
life-forms is not supported by all authors who classify
them as semi-aquatic or semi-terrestrial. Phytotelmatic
bladderworts grow in bromeliad cisterns that act as
drainoff free water storages (e.g. U. humboldtii).
Bladderworts are mostly small, herbaceous, annual or
perennial plants. Most species do not reach overall lengths
.30 cm but, as exceptions, some aquatic species such as
U. vulgaris can reach a length of up to 2.5 m. The basic
cormophyte organs, leaf and stem, cannot be clearly
distinguished, and roots are completely absent
1889; Lloyd 1942; Troll and Dietz 1954)
. Some aquatic
bladderworts develop dimorphic shoots
(Friday 1991; Adamec
In most bladderworts, the stem is elongated and termed
a stolon (Fig. 1A). This feature is absent in some
phylogenetically early-branching species (e.g. U. multifida). Stolons
are often glabrous or carry a multitude of glands. In
terrestrial, facultative epiphytic and facultative lithophytic
species, the stolons are very thin, only a few centimetres
long and form a dense network in the soil. In aquatic
species, the stolons are much thicker and longer, split up
and form a characteristic branching architecture
and Rutishauser 1990; Rutishauser 1993)
Leaves are developed in rosettes, whorls or dispersed
all over the stolons. In aquatic species, the classification
as a ‘leaf’ is often difficult, as these species often possess
. Nonetheless, the strongly
branched structures emerging from the stolons of these
species are termed as pinnate, filiform leaves
et al. 1989; Taylor 1989; Barthlott et al. 2007)
(Fig. 1A – D).
Bladderworts do not possess true roots, but some
species make use of root-like structures (rhizoids) for
anchorage. Rheophytic bladderworts cling to rocky
surfaces with specialized rhizoids that additionally
possess adhesive trichomes
(Van Steenis 1981; Taylor 1989)
Turions are produced when continuous growth is
inhibited, e.g. by seasonally cold temperature or drought
1906; Wager 1928; Taylor 1989; Adamec and Kucˇerov a´
The trap development takes place on different locations
on the plant body, i.e. on stolons, rhizoids or leaves. In
aquatic species, they mainly appear on leaves or leaf
segments, at the branching points of leaves, on side shoots of
stolons (e.g. U. naviculata) or at the leave bases (Fig. 1B– D).
They are constituted of a laterally flattened hollow
spherical body with a size between 0.2 mm and 1.2 cm
. Rheophytic U. neottioides is almost completely
devoid of traps
(Adamec et al. 2015)
. Some species (e.g.
U. vulgaris) feature a trap dimorphism in having two trap
morphotypes that differ considerably in size (Fig. 1B and
C). The bladders are connected by slender stalks to the
plant body (Fig. 1B – E). The position of trap opening (also
called the mouth) in relation to the point of stalk insertion
varies among species: traps possessing a so-called basal
position are characterized by a mouth situated directly
adjacent to a stalk (Fig. 2A), a terminal position is present
when the mouth is situated adversely to the stalk (Fig. 2B)
and all intermediate positions are classified as lateral
mouths (Fig. 2C) as it is the case in the here described
U. vulgaris trap type (Fig. 1E). The lower trap half with the
stalk insertion point is termed the ventral part, the upper
half of the dorsal part (Taylor 1989) (Fig. 2). Despite their
reduced chlorophyll content and low photosynthetic
efficiency, the bladders, which serve for the uptake of
growthlimiting plant macronutrients (nitrogen and phosphorous)
from prey, are physiologically very active and require great
Aquatic Utricularia capture a wide range of members of
Tardigrada, Nematoda, Gastropoda, Acaridae, Rotifera,
Ciliata and Crustaceae (especially Cladocera, Copepoda
and Ostracoda) (Figs 1E and 3A)
(Darwin 1875; Andrikovics
et al. 1988; Mette et al. 2000; Harms 2002; Sanabria-Aranda
et al. 2006; Gordon and Pacheco 2007; Guiral and Rougier
2007; Alkhalaf et al. 2009; Kurbatova and Yershov 2009)
Reports of large Odonata larvae
(Martens and Grabow
or even young fish
(Moseley 1884; Gudger 1947)
(Fig. 3B) as prey can most
certainly be considered as exceptions. Mosquito larvae,
which are also often too large for the bladders, are
commonly caught tails first with their heads sticking out
(Fig. 3C and D) (Brumpt 1925).
Płachno et al. (2014)
found diatoms in taps of the affixed aquatic U. volubilis.
Moreover, a multitude of other microorganisms (‘algae’,
bacteria and protozoa) can be found inside the traps,
which are part of complex (and not yet fully understood)
food-web relationships with the plants
Schumacher 1960; Peroutka et al. 2008; Alkhalaf et al.
2009, 2011; Sirova´ et al. 2009; Płachno et al. 2012; Caravieri
et al. 2014; Koller-Peroutka et al. 2015)
. For further reading
on this topic, see also the section about the functional
principle of the traps and the comprehensive reviews by
Adamec (2011a, b) as well as the references cited therein.
In contrast, little is known about the prey spectrum in
non-aquatic Utricularia species.
members of Rhizopoda, Crustacea and Acaridae in
Jobson and Morris (2001)
Insecta, Maxillopoda (especially Elaphoidella), Ostracoda,
Branchiopoda, Chelicerata, Eutardigrada and
Adenophorea (nematodes) as prey in U. uliginosa and
et al. (2002)
discovered in laboratory experiments that
Protozoa (i.e. Blepharisma americana) were attracted
and caught by several non-aquatic Utricularia species.
Functional Principle of the Traps
Mode of functioning of traps of the U. vulgaris type
The aquatic Utricularia trap works in two distinguishable
phases (Fig. 4A). It represents a hollow vesicle filled with
water, which is, in the first phase, actively pumped out of
the trap body by specialized glands (see also the section
about the functional morphology of traps of the U. vulgaris
type). Adaptive changes in the transmembrane protein
complex cytochrome c oxidase provide respiratory power
for this energy-demanding process that induces a lower
internal hydrostatic pressure in respect to the outer medium
(Sydenham and Findlay 1975; Jobson et al. 2004; Laakkonen
et al. 2006)
. Sasago and Sibaoka (1985a) determined
a pressure difference of 0.14 bar in U. vulgaris, and
et al. (2011)
measured a difference of 0.12 bar in
U. stellaris. Owing to the pressure difference and the
resulting underpressure inside the bladder, a
ready-to-catch trap shows concave curvatures (as seen
from the outside) of its lateral, flexible trap walls, which
by this store elastic energy (Figs 1D, 3A and 4). Large
traps can easily be manipulated manually to reset to a
deflated state by pressing the lateral trap walls, hereby
squeezing water out of the trap through the entrance.
In traps taken out of the water that fire in air, which is
accompanied by an audible clicking noise
the deflation process may become short-circuited owing
to air bubbles (Fig. 4B)
A trapdoor closes the trap watertight (Figs 1D and E, 3A,
and 4 – 8). Prey animals can trigger the trapdoor by
touching trigger hairs on the outer door surface, which entails
the second phase, comprising door opening in less than
half a millisecond, trap wall relaxation and water (and
thereby prey) influx due to the sudden increase of the
(Merl 1922; Lloyd 1942; Sydenham and
(Figs 4 and 9). In respect to trap movement
duration, Utricularia is by far the fastest carnivorous plant
(snapping in the Droseraceae D. muscipula (Venus flytrap)
and Aldrovanda vesiculosa (Waterwheel plant) takes
(Forterre et al. 2005; Poppinga and Joyeux
2011; Poppinga et al. 2013a)
, and snap tentacle catapult
movement in Drosera glanduligera takes 75 ms (Poppinga
et al. 2012)). Vincent et al. (2011b) measured in U. inflata
that the fluid inside the aspiration zone, which extends to
a distance of up to 500 mm from the trapdoor,
accelerates with up to 600 g and reaches a top speed of
1.5 m s21, leaving prey animals in the vicinity of the
entrance no chance to escape. The Reynolds number of
the fluid reaches 900, indicating a laminar flow.
Furthermore, prey often rotates and loops inside the trap in a
motion away from the entrance (Fig. 4C), which is
hypothesized to be crucial for retention of already caught
prey, which otherwise might become flushed out of the
trap. The suction-induced water swirl moves in opposite
direction to the trap entrance and thus is unlikely to
help in the door reclosing motion (see also the section
about the trapdoor movement). Probably, the more or
less triangular-shaped threshold and the overall lenticular
appearance of the trap (see also the section about the
functional morphology of traps of the U. vulgaris type)
dictate the swirl direction, whereas rotation of the prey is
likely induced by the shape of the animal.
The suction process can also be triggered manually by
tools such as human hair, fine wire or needles
1922; Merl 1922)
. After triggering, the elastic energy
that is stored in the concave trap walls is converted into
kinetic energy with the trap walls becoming convex (as
seen from the outside) during the second phase
(Fig. 4A). Due to the fact that piercing the trap, e.g. with
a fine needle, leads to a stronger outward (convex) trap
wall curvature than observed in an intact trap after firing
(Fig. 4D–F), it can be speculated that the pressure
difference does not become completely levelled by suction
(Lloyd 1935). The kinetics of this plasticity effect of trap
walls in opened traps has been described by Adamec
(2011d). This is in concordance with our own
investigations of high-speed videos of suction events which
indicate that the trapdoor is already reclosed before the
trap is fully inflated (i.e. before the trap walls are convex)
(Fig. 4G). According to this, the reset force of the door that
leads to closure (see also the section about the trapdoor
movement) exceeds the force of the water inflow at a
certain point, which effectively helps in preventing the
escape of prey.
Caught prey suffocates due to anoxia inside the bladder
(Adamec 2007b, 2010b)
. After being dissolved by
digestive enzymes secreted by glands on the inner trap surface
(see also the section about the functional morphology of
traps of the U. vulgaris type), the nutrients can be
absorbed by the plant. Both phases together form the
repeatable ‘active slow deflation/passive fast suction’
sequence (Fig. 4A) found in traps of aquatic Utricularia
(Czaja 1922, 1924; Merl 1922; Withycombe
1924; Hegner 1926; Gibbs 1929; Lloyd 1929, 1932, 1935,
1936a, 1942; Kruck 1931; Sydenham and Findlay 1973,
1975; Meyers and Stricklert 1979; Sasago and Sibaoka
1985a, b; Friday 1989, 1991; Adamec 2011c, d, 2012;
Singh et al. 2011; Vincent et al. 2011a, b)
The water is pumped out of the trap continuously and
probably recirculates as soon as a given pressure
difference is reached
. The outward flow is
hypothesized to be compensated by an inward flow
caused by trap wall permeability and/or trapdoor leakage
(Joyeux et al. 2011; Vincent et al. 2011a)
. The time for
resetting depends on the species studied (Meyers 1982)
and varies with temperature
age and, as for cut-off traps, the duration of storage
(Sydenham and Findlay 1973)
. The trap of U. vulgaris
is reset after 15 – 30 min. Traps are able to capture
multiple prey animals one after another:
observed 13 prey capture events within 3 days in a trap
of U. australis. Also, multiple prey animals can become
captured with one suction swirl. In contrast to the
snaptrap of the Venus flytrap (D. muscipula), no morphological
change (i.e. growth) is required in the Utricularia trap
for resetting and repeated trap firing
(Adamec 2011c, d, 2012; Vincent et al.
showed that aquatic Utricularia traps also fire
spontaneously without prey irritation after 5 – 20 h and
up to 60 times in a 20-day period. It is hypothesized
that, owing to the continuous process of water pumping,
traps can generate a sufficient pressure difference for
already (very) small mechanical perturbations
(mechanical/thermal noise) causing trap firing (see also the
section about the trapdoor movement). These
spontaneous firings occur trap-individually in different,
speciesindependent patterns: ‘metronomic traps’ fire regularly
after more or less fixed time intervals, ‘random traps’
show temporally scattered suction events and ‘bursting
traps’ display several rapidly succeeding firing events
separated by variable time intervals. The ecological
consequence of spontaneous firings for the plant is not yet
clearly solved. Probably, they prevent material fatigue in
the trap walls and, hence, traps to collapse. Moreover, a
multitude of microorganisms (‘algae’, bacteria, protozoa,
rotifers, etc.) can be found inside the traps that alone are
not capable of triggering suction
(Gordon and Pacheco
2007; Peroutka et al. 2008; Alkhalaf et al. 2009; Vincent
et al. 2011a, b)
but that could very well become
accumulated by spontaneous firings. These organisms are in
complex and not yet fully understood relationships with
the plants. Recently, Koller-Peroutka et al. (2015)
confirmed a prey biomass input by spontaneous firings,
which adds to Utricularia nourishment.
Functional Morphology of Traps of the
U. vulgaris Type
In aquatic bladderworts, the traps typically constitute
10 – 50 % of the total plant biomass
. In the following, the functional morphology of
traps of the U. vulgaris trap type is described in detail.
This trap type is characterized by an angle of 908
between the trapdoor and the threshold, as viewed in a
longitudinal section (Fig. 5). This is in contrast to other,
much less investigated trap types of non-aquatic species
that are concisely described in a separate section at the
end of this review (Fig. 10)
(Lloyd 1935, 1936a, 1942)
The trap body
The lenticular traps of species of Utricularia sect.
Utricularia are typically between 0.5 and 6 mm in diameter
(Taylor 1989; Adamec 2011d)
(Figs 1 – 5). Utricularia
reflexa may produce ‘giant’ traps that can reach up to
8 mm in size in culture (L. Adamec, pers. comm.).
The trap wall. The flexible trap wall mainly consists of two
cell layers (Fig. 5B and D). Both the inner and outer walls
are covered by a cuticle. The chlorophyll-rich cells are
more or less quadrangular as seen in longitudinal
section and elongated in transversal direction
. During the trap resetting phase, the lateral walls
bend inside owing to the underpressure inside the
bladder with the cells of the outer layer being
compressed. The outer cell layer is thicker, which can be
interpreted as a means for avoiding the trap to collapse.
Vincent et al. (2011b) estimated the stiffness of the trap
body to be in the range of 5 – 20 MPa, which is
concordant with values measured for fully turgescent
(Niklas 1988; Speck and
Vogellehner 1992; Speck 1994)
A single vascular strand (mostly phloem, sometimes
also xylem) runs through the stalk into the trap body,
here splitting up into two ‘branches’ that are arranged
along the trap profile
(Lloyd 1935, 1942)
. One branch
runs along the dorsal line of the trap until it ends at the
upper part of the trap entrance. The lower branch extends
from the stalk to the threshold, there splitting up once
more. From here on, both small vascular branches run
laterally, then upwards and parallel to the trap opening and
terminate in the ‘antennae’.
Glands on the outer trap surface. The spherically headed
glands covering the outside of the traps and the outer
surface of the threshold (Figs 5B and D, and 6) are
comprised of a basal, middle and terminal cell
and Seabury 1975)
. They are of uncertain function.
According to different authors, they might play a crucial
role in pumping water out of the trap
(Kruck 1931; Nold
1934; Sydenham and Findlay 1973)
or in mucilage
(Barthlott et al. 2007)
Fineran and Lee (1980)
and Fineran (1980, 1985) state that these external
glands, when being in the process of development,
absorb solutes from the surrounding water, which later
(after morphological changes of the glands) help in the
water-pumping mechanism during the trap resetting
phase. Owing to a negative periodic acid-Schiff
Thurston and Seabury (1975)
conclude that these
glands do not produce mucilage. These glands as well as
those situated on the trapdoor (see Figs 7 – 9) or the
substances released from them can both be stained by
Toluidine blue (Fig. 6A and B).
Glands on the inner trap surface. Two types of glands can
be found on the inner trap surface: two-armed glands
that possess two terminal cells (bifids) and four-armed
glands with four terminal cells (quadrifids) (Figs 5, 6C
and D, and 7D – F, I and J)
(Darwin 1875; Prowazek
. In some Utricularia species, these types of glands
are replaced by other gland types (Taylor 1989). The
epidermal basal cell is similar to the cells of the outer
trap surface but slightly smaller. The compact middle
cell typically resembles a disc or a dome. The intensely
cutinized lateral walls with attached cell membrane
suggest a barrier function for apoplastic transport into
the terminal cell
. Furthermore, the
middle cell features noticeable cell wall inversions at
the area of the outer transversal walls and upper half of
the lateral walls
(Fineran and Lee 1974; Fineran 1985;
Płachno and Jankun 2004)
. The glandular secretory
terminal cells of the bifids and quadrifids are regarded as
the most modified cells found among plant trichomes
(Fineran 1985), and the proximal regions of the ‘arms’
form a collective stalk with mechanically stabilizing,
markedly thickened outer walls
(Fineran and Lee 1975;
Fineran and Gilbertson 1980)
. The two terminal cells of
the bifids diverge at the distal part of the stalk, with each
of the cells forming one arm of the gland. The four terminal
cells of the quadrifids first form two opposite pairs that
subsequently diverge. The angle between the arms and
their general arrangement can be used for systematic
(Thor 1988; Cleal 1998; Doyle and Parnell 2003;
Yang et al. 2009)
. The cuticle of the terminal cells either
shows a discontinuous organization or ruptures during
gland ontogeny (Fineran 1985).
Bifids are densely packed near the trap entrance on the
inner surface of the trap body (Figs 5C and 6C). Every
epidermal cell in this region develops such a gland. The two
elongated terminal cells protrude into the trap interior
being perpendicular to the inner surface of the trap.
Quadrifids cover the rest of the inner trap surface (Fig. 5C). Each
gland is surrounded by epidermal cells and hence
separated from neighbouring glands. In contrast to bifids, the
terminal cells of the quadrifid glands are arranged parallel
to the inner trap surface.
The glands are responsible for pumping water out of
the trap body, for secretion of digestive enzymes and
for absorption of nutrients. Until now, it is not yet entirely
understood what gland type fulfils which function.
quadrifid glands pump water out of the trap, a hypothesis
that has not been rebutted until today
Kruck 1931; Nold 1934; Fineran and Lee 1975; Fineran
and Gilbertson 1980)
Fineran and Lee
postulate that the quadrifids are responsible for
water transport together with the spherical glands on
the outer trap surface.
Fineran and Lee (1975)
that the bifid glands help in the water-pumping process.
Sydenham and Findlay (1975)
and Sasago and Sibaoka
(1985a) on the other hand postulate that the quadrifids
serve the purpose of prey digestion and nutrient
absorption. According to them, the pumping of water is
performed by the bifids in cooperation with the glands of
the pavement epithelium in the outer and middle zones
that act as the outlets for the water outflow. This
conclusion is due to the fact that water emerges exclusively next
to the trap entrance (this observation was made with a
trap resetting in paraffin oil) and as the bifid glands
with their not cuticle-covered terminal cells are situated
near this region. This separation of function between
the two types of glands has not yet been verified but is
considered as the current state of research in literature
(cf. Juniper et al. 1989; Barthlott et al. 2007)
(1942) furthermore hypothesized that bifids also hinder
caught prey animals to pass the threshold and to escape.
Although the hypothesis that the quadrifids are fully or
partly responsible for prey digestion and nutrient uptake
dates back to
and von Goebel (1891), little
is known about the process of digestion in Utricularia.
Since the 1970s, cytochemical investigations of
quadrifids revealed that protease
(Vinte´ joux 1974; Vinte´ joux
and Shoar-Ghafari 2005)
, acid phosphatase and esterase
(Heslop-Harrison 1975) are secreted. Recent studies by
Sirova´ et al. (2003)
and Adamec (2010a) focussed on
activities of extracellular enzymes (e.g. phosphatase).
The trap entrance
Appendices at the trap entrance. At the trap entrance,
several types of appendices occur which differ in number
and structure and are of taxonomic importance
1989; Reifenrath et al. 2006)
(Figs 1D and E, 3A and D,
4D – G, 5, and 6A and C). Darwin (1875) termed the two
multicellular and branched structures emerging from the
upper edges of the trap entrance as ‘antennae’ and the
filamentous, non-branched structures situated laterally
on the trap entrance as ‘bristles’. Darwin used these
terms because the overall shape of a trap reminded
him of small aquatic crustaceans like Daphnia. With
investigations on aquatic U. vulgaris,
Meyers and Stricklert
could confirm Darwin’s hypothesis that ‘antennae’
covered with epiphytic algae
(Prowse 1959; Guiral and
enhance Utricularia’s capture success by
guiding substrate-dwelling prey animals towards the trap
entrance owing to their funnel-like arrangement (Figs 1E,
3A and 4G).
The threshold. The lower part of the trap entrance is
constituted of a massive, collar-like tissue, which is
bent upwards and termed threshold
(von Goebel 1891)
(Figs 1D, 3A, 4D–G, 5, 6, 7I, 8C and 9B). In longitudinal
section, it resembles an upside-down triangle that merges
into the trap wall (Figs 5 and 6). In its spatial dimension, it
comprises four to five rows of parenchymatous cells and is
surrounded by a layer of approximately isodiametric
epidermal cells on each side, i.e. towards the interior and
exterior of the trap
. The threshold surface is
undulated owing to varying sizes of the epidermal cells
and of the parenchymatous cells underneath (Fig. 6B
and D–F). At the lateral transition area connecting the
threshold and the trap wall, the epidermal cells increase
in size and merge into the inner and outer cell layers of
the trap wall (Fig. 5B). At this transition zone, the trap wall
is relatively thin by which deformation of the threshold
owing to the underpressure-induced deformation of
the trap walls is avoided. The threshold mechanically
stiffens the entrance and reduces deformation during the
resetting phase and during suction. Independent of the
physiological trap condition, it maintains its geometry and
helps ‘framing’ the door, which is sensitive to mechanical
perturbations (see also the section about the trapdoor
The threshold surface is slightly convex and can be
divided into an outer, middle and inner region
1942; Juniper et al. 1989)
(Fig. 6D – F). The outer region
represents part of the entrance corridor and comprises
epidermal cells, which sometimes carry stalked glands
(Figs 5B, and 6D and F). The inner region of the threshold
also consists of epidermal cells and forms a nose-like
structure that extends into the trap (Figs 6B, D and F,
and 7J). It is considered as being part of the inner trap
surface. The middle region (Fig. 6D – G) is constituted of
tightly packed, short glands forming a specialized
glandular tissue on which the door rests. According to its visual
appearance—the glandular surface resembles a cobble
stone pavement—von Goebel (1891) termed it the
‘pavement epithelium’. Alike the stalked glands that can
be found on the trapdoor and in the entrance zone, those
of the pavement epithelium consist of three cells
(epidermal basal cell, endodermal middle cell and glandular
(von Goebel 1891; Lloyd 1942; Thurston and
Seabury 1975; Fineran 1985)
. During ontogeny, the
cuticles separate from the terminal cells and become shed.
According to Lloyd (1932, 1936a, 1942), three
pavement epithelium zones (outer, middle and inner zone)
can be distinguished by gland morphology (Figs 6E – G
and 7J). These three zones are all parts of the middle
region of the threshold surface. The outer zone is
characterized by glands with cuticles, which are bloated like
balloons. Cuticles from glands of the middle zone become
shed but stick together and with the cuticles of glands
of the outer zone. The resulting filigree, transparent,
membranous structure is termed velum
(Figs 5B, 6C – F, and 7I and J). It consists of two parts:
the cushion-like structure of connected balloon-like
cuticles that run along the whole outer region and, connected
to this cushion, the membrane emerging from cells of the
middle region. The putatively ‘sticky’ (see below) velum is
hypothesized to cling to the free edge of the closed
trapdoor and hence to play a mechanical role in trapdoor
movement and to help for maintaining the trap sealed
(Lloyd 1935, 1942; Broussaud and Vinte´ joux
1982; Fineran 1985)
. Kurz (1960) argues that the velum
consists of swollen cell membrane without cytoplasm,
suppose the velum to consist of a stretched protocuticle.
The gland heads in the middle zone possess a soft surface
(owing to the shed cuticle) in which the lower free edge of
the trapdoor can subside. The inner zone of the pavement
epithelium is broadest in the middle of the threshold and
becomes thinner more laterally, as viewed from above
(Fig. 6G). Here, the glands are larger and less densely
packed as in the two other zones. Their cuticles also
detach from the cells but mostly rupture. It is still not
solved which mechanism leads to cuticle detachment,
but probably it may be due to cell exudation. Glands on
the pavement epithelium are supposed to secrete a
(Cheema et al. 1992)
, which helps
for sealing the trap entrance watertight
1924; Fineran 1985)
and/or for lubricating the entrance
to ensure a smooth door movement (Lloyd 1942).
The threshold exhibits two bumps on its surface: a
larger elevation comprising the outer and middle zone of the
pavement epithelium and a more shallow elevation at the
inner zone (Fig. 6E and F). The cavity between these two
bumps acts as a furrow for the free door edge in its closed
state (Figs 6F and 8C). At the bottom of this cavity, there is
the transition between the middle zone to the inner zone
of the pavement epithelium, and the door edge rests on
the flexible gland heads of the middle zone. In a
ready-to-catch trap, the outer door edge surface presses
against the slopy edge of the anterior bump. An inward
swinging (opening) of the trapdoor is prevented by a
second, more shallow bump. Despite the water pressure
acting on the door, the door edge cannot pass this
bump without previous trigger-induced deformation
and slight displacement from the surface (see also the
section about the trapdoor movement).
Glands at the trap entrance. The lateral and ventral inner
surface of the trap entrance, near to the pavement
epithelium, is covered with long-stalked pyriform glands
resembling those on the upper part of the middle region
on the door (Figs 5B and D, 6B–D and F, and 7C, E and I).
The lengths of their basal cells decrease in direction to
postulated that these glands
absorb substances, alike the quadrifid glands covering the
inner trap body surface, which are released during the
process of digestion. In addition, they were suspected to
attract prey animals
(Cohn 1875; Bu¨ sgen 1888; von
Goebel 1891; Kurz 1960)
. Thurston and Seabury (1975),
by investigating U. biflora, attributed mucilage production
to these glands as well as to the stalked glands on the
trapdoor and to the bifid and quadrifid glands, owing to
positive periodic acid-Schiff staining and due to the
gelatinous and filamentous substances sticking on the
terminal gland cells. In contrast,
Fineran and Lee (1980)
could not detect mucilage secretion by the stalked glands
in the entrance zone of terrestrial U. dichotoma.
and Findlay (1975)
hypothesized that the water taken up by
the bifid glands is released to the trap exterior by the
stalked glands of the entrance zone or by glands of the
pavement epithelium, but the fact that not all Utricularia
species possess stalked glands in the entrance zone
makes this assumption unlikely
The trapdoor. The semi-circular trapdoor is a 20 – 40 mm
thick flap-like structure constituted of two cell layers
which closes the trap mouth watertight (Figs 5, 6B – D
and F, 7, and 8C). The door is fixed laterally to the trap
wall and to the upper part of the trap entrance along a
curved arch, hence retaining a free lower edge (Fig. 7A
and C – F). The free edge has a pointed tip which can be
seen in longitudinal section (Figs 6C, D and F, and 7B and
I) and is thicker in the middle part of the door than in its
lateral parts. The door shows an outward curvature when
it is closed and when the trap is ready to catch (Figs 8C and
9B). The outward curvature is inter alia due to the fact that
the free edge of the trapdoor is longer than the contact
area on the pavement epithelium (Fig. 6G) (see also the
section about the trapdoor movement). Owing to the
collar-like appearance of the threshold, the angle between
the free trapdoor edge and the pavement epithelium
changes along this contact area. In the middle area, the
door rests in an approximate right angle on the pavement
epithelium, which changes to increasingly acute angles in
the more lateral regions. At the outermost parts, the
surfaces of the trapdoor are in contact with the pavement
Regions on the trapdoor. According to
trapdoor can be compartmentalized into four regions
(Figs 7B, D, F and H, and 8B and C): the hinge region, the
middle region, the central hinge and the middle piece.
The hinge region comprises a broad zone along the
connection between the door and the trap wall, thereby
surrounding the middle region, the central hinge and the
middle piece. It can be subdivided into two mechanically
relevant parts: one upper hinge and two lateral hinges.
When the trapdoor is closed, the upper hinge shows an
inward curvature (Figs 7B and 8C), which is strongest in
the middle of the trapdoor and is most pronounced in
the set condition. The lateral hinges comprise the zones
at which the door moves back and where the outer door
surface partially rests on the pavement epithelium. The
central part of the door (inter alia comprising the middle
region) shows an outward curvature in contrast to the
upper hinge, i.e. it is convex when seen from the outside
(Figs 7B and 8C). On the middle of the trapdoor’s lower
edge, there is a circular area, the central hinge, where two
of the four trigger hairs are located. Here, the trapdoor is
comparably thin. Below the central hinge, the middle
piece is located (Fig. 7H). Here, the lower trapdoor edge
is thick and stiff, and on its outer surface, the other two
trigger hairs are located. The central hinge, the middle
piece and the areas on the lateral hinges that are
situated below the middle region show a convex
curvature, when seen from the outside in the set
posture, and have the approximate shape of the quarter
of an ellipsoid surface (Fig. 8C).
The inner layer of the trapdoor consists of elongated
cells that have been described to function as compressive
(Lloyd 1942; Juniper et al. 1989)
and are radially
arranged around the central hinge (Figs 7D, F and H, and
8B). Constrictions of these cells appear as patterns of
circular lines in the middle region of the trapdoor and
presumably increase its flexibility in radial direction, hereby
acting as prefolds for channelling the reproducible door
opening and closing
(Lloyd 1942; Juniper et al. 1989;
Vincent et al. 2011b)
(see also the section about the
trapdoor movement). The cells of the hinge region along the
trap wall are not constricted and might act as a spring
structure for door closure. The smaller cells of the outer
door layer are not distinctly compartmentalized (Figs 7C
and E, and 8A). Vincent et al. (2011b) also noticed lateral
trapdoor folds (Fig. 7C – G) that are hypothesized to add
displacement space during suction of prey by unfolding,
to ease and channel the in- and outwards bending of
the trapdoor and to allow for positioning the relatively
long free trapdoor edge on the pavement epithelium
permitting a watertight closure.
Histology of the trapdoor. From an anatomical point of
view, the trapdoor is a continuation of the trap wall and
hence analogically constituted of two cell layers (Fig. 7B).
The relative thickness of the layers varies with the function
of the respective door region. In many parts (hinge
region and middle piece), the outer cell layer is up to
three times thinner than the inner layer. Exceptions are
the central hinge and the middle piece where both layers
are approximately of equal thickness. Large differences in
thickness of the two cell layers mainly occur in door regions
that take mostly part in the door movement and hence
must be flexible. At the central hinge, the trapdoor is
thinnest ( 13– 16 mm in U. vulgaris).
The inner and outer cell layers of the trapdoor also
differ according to their general structure. The outer cell
layer consists of tabular cells with anticlinal borders
running in a wavy or zigzag pattern
(Bu¨ sgen 1888; Lloyd
(Fig. 8A). The curves and corners of the
borders possess, according to the respective region of the
trapdoor where they are situated, more or less
pronounced reinforcing ridges, which prevent collapsing
of the respective cells during deformation. In the upper
hinge, and partly also in the middle piece and in the
lateral hinges, the cells are more or less isodiametric and the
anticlinal borders also follow a zigzag pattern and
possess reinforcing ridges
(Cohn 1875; Lloyd 1932, 1942)
In direction to the outer surface of the lateral hinges,
the corners become more and more roundish and the
anticlinal borders adapt to a wavy pattern. The cells
here are transversally elongated, do not possess
reinforcements and run parallel to the free door edge. The outer
cells of the central hinge, however, are very small, nearly
isodiametric and feature many reinforcing ridges that
form a complex pattern. In the middle piece, the outer
cell layer also features very small, isodiametric cells
with reinforcing ridges forming a bilateral symmetric
. Hence, the outer door regions, e.g. the
hinge region, which become strongly deformed during
the door movement, are characterized by cells with
zigzag anticlinal borders and small reinforcing ridges,
whereas the stiffest region (middle piece) exhibits the
thickest cell walls and a multitude of noticeable
The inner cell layer of the trapdoor (Fig. 8B) in the
middle and hinge regions consists of elongated cells that run
radially. Their size increases with the distance to the
central hinge. The anticlinal borders are thin, run in a zigzag
or wavy pattern and possess many reinforcing ridges. The
periclinal walls facing the trap inside are, in contrast to
the anticlinal borders, much thicker. Moreover, the inner
cells are constricted in a constant fashion perpendicularly
to the inner door surface. These constrictions run along
several cells, seldom conforming to the transversal cell
hypothesized that the constrictions follow the transversal walls
and described the cells as isodiametric (Fig. 8B). Hence,
the periclinal cell walls are characterized by several
convex curvatures with cell borders that may run across the
apex of these bulges. At the zones where the
constrictions meet the anticlinal borders, reinforcing ridges or
plates are developed. In the inner part of the middle
piece, the constrictions run concentrically around the
central hinge. Irregularities only exist near the
longitudinal axis and near the free edge of the trapdoor where
the constrictions furcate. In the upper and lateral hinges,
the constrictions are less noticeable than in the middle
region. The cells of the central hinge and of the middle
piece are very small and isodiametric, and the inner cell
walls are characterized by a multitude of reinforcements.
The periclinal cell walls of the central hinge also feature
constrictions, which in contrast do not run only
concentrically but also perpendicularly in radial direction. In
the middle piece, there are no constrictions, but the
periclinal borders are much thicker than in the other door
(Lloyd 1932, 1942)
Due to the above described structuring, the
two-cell-layer-thick trapdoor regions possess different
mechanical bending and stretching properties. Despite
both being turgescent, only the cells of the inner layer
deform noticeably in the middle and hinge regions
(Lloyd 1942; Juniper et al. 1989)
. Such a bilayer structure
further entails that the door can only move towards the
trap inside. A manual outward pressing leads to a rupture
of the trapdoor because it is tightly framed in the trap
entrance. When the trapdoor is cut-off from the entrance,
it will instantly flip outwards and will only reset by
plasmolysis. According to this scenario, the door most likely
is under tension by turgor in its resting position.
Presumably, the structural differences in the various trapdoor
regions contribute to the tension that helps keeping the
door in its resting position on the threshold and to enforce
the door closing after prey capture (see also the section
about the trapdoor movement).
Glands on the trapdoor. The outer door surface is covered
with a multitude of glands of different types. In the upper
part of the middle region, there are situated several
long-stalked, three-cellular glands with pyriform terminal
cells (Figs 5, 6A–C, and 7B, C, E and I). They form a broad,
band-like seam along the transition zone between the
upper hinge and the middle region. Near the free
trapdoor edge three-cellular stalked glands with spherical
terminal cells are found (Figs 7C, E, H and K, and 8A). The
stalks of these glands are much shorter than those
found in the pyriform glands and their terminal cell is
much larger in relation to the stalk diameter. These
short-stalked glands form a row that runs parallel to the
free trapdoor edge underneath the trigger hairs and
reaches up to the lateral hinges. They are arranged in a
manner alternating to the trigger hair bases, and the
central gland is larger than the rest. Between the trigger
hairs and the long-stalked glands, the middle region of
the trapdoor often is covered by two-armed, sessile
(Fig. 7B, C and E; Darwin 1875)
. The function of
these glands is not yet known, and it is speculated that
they may play an important role in either absorption or
(Darwin 1875; Bu¨ sgen 1888; Meierhofer
1902; von Luetzelburg 1910)
Trigger hairs. Mostly four stiff, pointed and long trichomes
protrude from the central lower part of the trapdoor
(central hinge and middle piece) (Figs 1E, 6C and D, and
7A – C, E, I, K and L). These trigger hairs are arranged as
stacked pairs in the form of a rectangle or a slightly
shifted trapezoid. They are constituted of three to up to
five elongated cells with an increasing cell length from
the basal cell to the top
. They are inserted
obliquely to the door and anchored in the outer
trapdoor cell layer with a bulged basal cell
1902; Merl 1922; Lloyd 1942)
(Fig. 7L). Some Utricularia
species (not of U. sect. Utricularia) are lacking trigger
hairs but feature stalked glands (e.g. U. cornuta and
U. purpurea) or other types of trichomes
Mechanical stimulation of one of the trigger hairs leads
to trapdoor opening and suction of water, independent of
the direction of the stimulus. According to
manual triggering is ‘easier’ when performed laterally or
from above. Two hypotheses exist on how the trigger
hairs work. The mechanical hypothesis postulates that
the hairs act as levers
(Czaja 1922; Merl 1922; Lloyd
1932, 1935, 1942)
. A trigger hair bending deformation
owing to contact by prey is transduced to the middle
piece of the trapdoor which also deforms, resulting in a
slight displacement of the free trapdoor edge on the
pavement epithelium and causing it to pass over the
barrier bump (see also the section about the trapdoor
movement) (Fig. 6E and F). The trapdoor can no longer resist
the water pressure and opens. According to the
physiological hypothesis, the trigger hairs are analogues to
the sensory hairs of the Venus flytrap (D. muscipula)
and waterwheel plant (A. vesiculosa) (both Droseraceae)
(Brocher 1912; Ekambaram 1924; Withycombe 1924;
Kruck 1931; Diannelidis and Umrath 1953; Sydenham
and Findlay 1973; Broussaud and Vinte´ joux 1982)
this scenario, a mechanical stimulus on the hairs results
in the generation of an electrical signal that is transduced
over the trapdoor and leads to cell contraction
, respectively turgor changes
followed by trapdoor deformation and finally trapdoor
opening. None of these hypotheses could be verified
until now, and
Juniper et al. (1989)
suppose that both
might hold true for at least some Utricularia species.
showed that diethylether, a membrane
ion channel inhibitor, and sodium azide, a cytochrome
oxidase inhibitor, as well as cold temperature (2 8C)
negatively influence the physiological processes involved in
trap resetting but not triggering, which gives support to
the mechanical hypothesis.
The suction of water and prey relies on a trapdoor that on
the one hand reliably seals the trap watertight (in the
resting position) and on the other hand performs an
ultra-fast and reversible opening and closing movement
(during the suction process). The structural prerequisites
described allow for the complex motion pattern of the
trapdoor, which is described in the following.
Trapdoor position before suction
In a ready-to-catch trap, the force exerted on the door due
to water pressure difference is levelled by the friction force
exerted by the pavement epithelium on the free trapdoor
edge. The outwards curved (convex) door is in a
(‘unstable equilibrium’, cf. Brocher 1912)
Its free edge becomes firmly pressed against the middle
zone of the pavement epithelium (Fig. 6F and G). The free
edge of the trapdoor rests with its outer surface on the
bulged outer zone of the pavement epithelium and its
lateral zone rests on the threshold (Fig. 8C). Beneath the five
short-stalked glands on the trapdoor, the velum closes the
gap between trapdoor and threshold along the connection
(Figs 6F and 7I). It is still unclear how
the lateral folds are positioned in the closed door in a
ready-to-catch trap as well as how they unfold during
the opening. Furthermore, the question of how notch
stresses are (probably) structurally avoided in these folds
remains to be answered.
Trapdoor opening and closing movement
The tiny traps of bladderworts and the high speed of their
trapdoor movement beyond human visual perception
impeded detailed analyses of their movements for a long
time. However, the early investigations by Ekambaram
Sydenham and Findlay (1973)
are quite noteworthy. Despite their mostly
hypothetical character, the results presented are close to
the much later described kinematics derived from
highspeed cinematographic analyses. In detail,
states that touching the trigger hairs results in a slight
deformation of the middle piece of the trapdoor and a
concomitant displacement on the threshold. Based on the
observation that the free door edge is longer than the
threshold (Lloyd depicts a length ratio of 110 : 100), he
concludes that it must deform in its middle zone (in the area of
the middle piece) to be able to pass the inner bulging of the
pavement epithelium. By using a bent wire, he physically
simulated the deformation of the free trapdoor edge and
showed that its curvature completely inverts during
trapdoor opening. Moreover, he states that the trigger hairs
collapse and flap against the outer trapdoor surface
(Fig. 9A). The closing movement of the trapdoor after
prey capture starts when the influx of water flow
diminishes and is owing to the intrinsic mechanical
properties of the trapdoor.
Quite recently, high-speed cinematography allowed for
recording and analysing the trapdoor kinematics in full
(Vincent et al. 2011b)
. The trapdoor first
inverts its curvature after triggering (with the trap still
being closed) (Fig. 9B). This quick deformation is a
snapbuckling process (or snap-through transition) that starts
in the thickened middle piece of the trapdoor below the
central hinge and is concomitant with converging trigger
hairs flapping against the trapdoor (Fig. 9A). The trigger
hair movement is due to the morphology of the trapdoor
in the areas of the trigger hairs insertion. Here, the free
trapdoor edge is thickened, which is visible in form of
bulges on the outer and inner trapdoor surface (Fig. 7H
and K). These thickenings are interrupted in longitudinal
direction by an area in which the trapdoor is very thin. At
this special area, the initial buckling (after triggering)
causing trigger hair movement takes place. The buckling
proceeds all over the trapdoor until the door inverts its
curvature completely. After this fast snap-buckling, the
trapdoor swings open in 0.5 ms (as measured on
average for U. inflata and U. vulgaris) and then recloses by
regaining its original curvature (unbuckling and
concomitant unfolding of the trigger hairs) within 0.5 – 300 ms
(Fig. 9). In a figurative sense, the first step after triggering
(trapdoor buckling) can be regarded as an ‘unlocking’ of
the trapdoor because once in the buckled position
(concave trapdoor curvature), it cannot resist the water
pressure any longer and swings open. As long as the suction
flow force is high enough (i.e. higher than the intrinsic
reset force of the trapdoor), the trapdoor remains open.
The closing of the trapdoor is often much slower than its
opening as it is solely driven by the reset force of the
trapdoor and is presumably not supported by the release of
elastic energy stored in the trap body and the water swirl
inside the trap (see also the section about the functional
principle of the traps). The trapdoor, which does not
move like an articulated flap but rather than an entirely
deformable elastic thin shell, was computationally finite
element modelled by Joyeux et al. (2011) (Fig. 9B). These
simulations confirmed the experimentally observed
complex kinematics, i.e. a rapid curvature inversion of the
trapdoor before opening.
Llorens et al. (2012)
dynamical model incorporating the whole trap. A
simplified physical door hand model for educational purposes
was developed by Poppinga et al. (2013c) (Fig. 9B).
Interestingly, snap-buckling as a movement principle has
been initially described for the trapping motion in the
Venus flytrap (D. muscipula)
(Forterre et al. 2005)
a one-way buckling leads to the fast trap movement
(whereas in Utricularia both buckling and unbuckling are
essential for a trap to function).
Trapdoor position after suction
During prey capture, a partial pressure equilibration takes
place between the trap inside and outside (see also the
section about the functional principle of the traps).
Afterwards, the water pressure acting on the trapdoor is lower
than in the ready-to-catch state. Hence, the trapdoor
takes a position which is dictated more by its architecture
than by water pressure, and therefore, its shape is more or
less convex (as seen from outside). Its lower free edge
also rests on the pavement epithelium, but closer to the
outer border than in the ready-to-catch trap state.
Despite the lower pressure difference between the trap inside
and outside, the relaxed trapdoor and the velum both
close the trap body watertight
Implications of the trapdoor buckling scenario
By the above-mentioned buckling scenario, the
mechanical reasons underlying spontaneous firing as well as the
triggering mechanism can be (partly) explained. With
the traps continuously pumping water out, the internal/
external trap pressure difference comes close to a critical
pressure for spontaneous trapdoor buckling and suction,
which may happen owing to thermal or mechanical
noise. Hence, the mechanical sensitivity of the trap
increases with the pressure difference. Shortly after
firing, the difference is not high enough so that mechanical
perturbations on the door do not lead to buckling and
(cf. Adamec 2011c)
. After 15 – 30 min, the
pressure difference is high enough again, so that mechanical
perturbations (together with the water pressure acting
on the door) entail trapdoor buckling and trap firing.
This scenario supports the hypothesis of mechanical
trapdoor triggering described in the chapter about the
trigger hairs, where a minute trigger hair displacement
(which acts as a lever) leads to a slight trapdoor
deformation that entails buckling. The physiological hypothesis
is herewith not yet ruled out, as the inactivity of traps
shortly after firing could also represent a physiological
refractory period. Finally, when the pressure difference
reaches a critical value of 0.155 bar
(as calculated by
Vincent et al. 2011a)
, the trapdoor buckles
spontaneously and the trap fires. However, by none of these
hypotheses, the burst firing observed in some traps
(see also the section about the functional principle of
the traps; Vincent et al. 2011a)
can be explained.
Probably, this firing type is caused by a variable position of
the trapdoor edge after each firing on the sealing
pavement epithelium, which could explain why a different
critical underpressure is needed for firing of the same
trap in the course of time.
Vincent et al. (2011b) proposed a general
architectonical ‘law’ for suction traps, taking the trapdoor buckling
scenario into account. Too thick and stiff a trap body
would not deform enough and would suck only a little
amount of water, and too soft a trap body would be too
slow during the passive fast suction phase. For an
optimized trapdoor to open at a stage of maximum trap
deflation (so that the trap can suck a maximum amount
of water and prey), it must be considerably thinner than
the respective trap body. The consideration of such a
door-to-body-thickness ratio may be helpful to estimate
trapping behaviour in Utricularia species where the
suction mechanism is doubtful owing to morphological
peculiarities, e.g. due to having exceptionally thick
(Reifenrath et al. 2006)
. However, thick and stiff
traps have recently been found in some Australian
Utricularia species from the Pleiochasia section (Płachno et al.
A Comparison of the Different Trap
Entrance Types in Utricularia
Knowledge on trap function and especially trapdoor
movement of non-aquatic Utricularia species is still
limited, because the respective traps are difficult to
investigate due to minor size and a multitude of obstructing
appendages around the trapdoor. The most detailed
examinations on the entire genus Utricularia were
conducted by Lloyd, who distinguished between short and
long tubular trap entrance types
(Lloyd 1936a, 1942)
and defined in the latter two variants, in which the
shape of the relaxed and curved trapdoor either can be
circumscribed by one continuous bend or by two bends.
In the short tubular trap entrance type, the angle
between the trapdoor in its relaxed posture and the
pavement epithelium measures 908. This is referred to as the
U. vulgaris trap type, which is described in detail in this
review. In contrast, long tubular entrance traps are
narrower and exhibit a narrow angle of 308 between the
trapdoor and the threshold (Fig. 10). Conspicuously,
species of the U. vulgaris trap type are aquatics, whereas
many non-aquatic species belong to the narrow-angled
type. However, Lloyd did not find a consistent correlation
between entrance types and the sections or species,
respectively. Since the morphological traits of the aquatic
section Utricularia have been described in detail in this
review, the focus in this section is on the long tubular
entrance type, which is common in non-aquatic species,
such as U. dichotoma, U. caerulea and U. cornuta. In this
type, the trapdoor is longer (from the hinge region to the
free edge) than broad (length of the free edge), thicker
than in the U. vulgaris type and possesses a massive
middle piece. In the set position, these trapdoors are
concave, in contrast to the convex trapdoors found in
U. inflata and U. vulgaris. Due to the underpressure inside
the traps, the trapdoor (which is in an oblique angle
towards the trap lumen) is pressed on the threshold,
which is aided by the stiffness of the lateral hinges and
by a concavity. The trap is additionally sealed by a
. Upon his detailed anatomical
examinations in U. bisquamata, Lloyd (1936b) concluded that
along the axis of the trapdoor, there is a very narrow
region of greater flexibility, so that during opening, a
momentary sudden longitudinal bending occurs, leading
to a reversal of the curvature. In the relaxed position, the
trapdoor is convex, the angle between trapdoor and
pavement epithelium is increased and the trapdoor becomes
watertight again. Over the course of resetting, the
trapdoor gradually returns to the concave set position. Many
non-aquatic species, for example the entire section
Pleiochasia, are devoid of trigger hairs
(Lloyd 1942; Taylor
1989; Reifenrath et al. 2006)
, which leaves the question
how they can be stimulated. The phylogenetically
earlybranching species U. multifida possesses a very thick
trapdoor, so that Reifenrath et al. (2006) suspect that it cannot
perform low-pressure suction movement altogether (see
also the section about the trapdoor movement). Due to
the extremely rapid trapdoor movement of bladderworts
and the lack of modern equipment, Lloyd was not able
to perform a detailed investigation on the exact opening
procedure in the long tubular entrance type. Surprisingly,
despite the high structural differences within the trap
entrances, the functional principles of the trapdoor
movement in non-aquatic Utricularia have not been subject to
Promising Aspects for Future Studies
Although we already have a detailed knowledge on the
function of the bladderwort traps, there remain
numerous intriguing questions of which some are decades old
and still remain unanswered. First, since the
comprehensive works by Lloyd in the 1920s– 40s, there have not been
conducted detailed analyses of the trap and trapdoor
motions in Utricularia species outside of section
Utricularia (see also the foregoing section). Such species
possess different door-to-threshold angles, tubular
entrances, different door-to-body-thickness ratios, other
structures for prey attraction, trigger hairs and they
probably have divergent prey spectra
(cf. Reifenrath et al.
2006; Albert et al. 2010)
. We believe that experimentation
in the laboratory, as well as in the field, with this highly
diverse genus would lead to a multitude of new insights
on trapping mechanisms, especially in regard to trap
architecture and probably prey diversity.
One of the oldest questions is how does the triggering
work? The trigger hair sensory cells in the Venus flytrap (D.
muscipula) are very well investigated and are
characterized by spirally running, concentric endoplasmatic
reticulae (ER) at the respective poles, which surround large
vacuoles filled with phenolic substances.
hypothesize that these ER complexes
function as pressure transmitter by causing a release of
the phenolic substances upon mechanical deformation.
Probably, investigations on trigger hairs of Utricularia
species using a transmission electron microscope (TEM) will
shed light on similar or different cellular architecture
enabling or excluding a physiological sensitivity.
Furthermore, electrophysiological experiments (e.g. electrical
irritation, measurements of the ion distribution with
microelectrodes and of turgor pressure) could help
elucidating the question if triggering of the trap is purely a
mechanical process or not
(cf. Adamec 2011a)
detailed microscopic studies of the middle piece and
more generally on the lower free edge of the trapdoor
with high-speed cameras capable of high physical
(pixel) resolution combined with high temporal resolution
(recording speed .10 000 fps) should allow for
comparative analyses of the kinematics of the trapdoor motion
during spontaneous (un-triggered) firings and in
manually triggered traps. With such a detailed analysis, it
might be possible to determine whether the
displacement/initial movement of the trapdoor always follows
the same pattern (which would speak for the involvement
of an electrophysiological step) or whether small
differences occur (which would speak for the mechanical
Furthermore, direct investigations in situ on
spontaneous firings, and how they might be ‘controlled’ by certain
environmental factors, have not yet been conducted.
With mobile and waterproof time lapse cameras, the
temporal patterns of spontaneous firings under natural
conditions can be monitored, and the intake of biomass
per trap could be quantified.
Until now, the process of water pumping out of the trap
is not yet fully understood. Tracer experiments with heavy
water or low-molecular/fluorescent dye could help in
elucidating the pathway of water out of the trap.
Moreover, the function of the glands on the trap entrance,
on the trapdoor and on the trap body is still unknown.
Detailed anatomical analyses (e.g. with TEM) and
selective staining of the substances secreted are necessary to
gain further knowledge of these structures.
Underpressure measurements in a high temporal
resolution are indispensable for determining the physical
boundaries for deflation, door buckling, successful prey
capture and spontaneous firings. Non-invasive
measurements (optical quantification of changes of trap width,
observation of air bubbles inside the traps) are still very
difficult to perform, but are in principle possible.
A challenging task is also the elucidation of how the
lateral flaps on the free trapdoor edge take part in the
overall trapdoor movement, i.e. to answer the question
whether they provide additional space by unfolding into
the trap. For building up the underpressure inside the
trap, which is necessary for trap firing, the traps must
remain unharmed, so that it is not possible to record a
manually evoked trapdoor motion in a sectioned trap.
One would need fine borescopes or similar optical devices
inserted into the traps combined with a very
lightsensitive high-speed camera to record the trapdoor
motion from inside the trap. Probably, the exact position
and arrangement of the flaps could be analysed
microscopically if the trap could be fixed in the ready-to-catch
state by chemical or other means.
Last but not least, the suction trap of Utricularia could
act as a role model for biomimetic suction devices
capable of repeatable ultra-fast collection of small amounts
Sources of Funding
We thank the German Federal Ministry of Education and
Research (BMBF) (funding directive BIONA, 01RB0806)
for long-lasting financial support. The current work is
funded by the Innovationsfonds Forschung of the
University of Freiburg and by the German Research Foundation
within the Cooperative Research Center CRC 141
‘Biological Design and Integrative Structures’.
Contributions by the Authors
All authors were involved in literature research and
reviewing. S.P., C.W. and A.S.W. recorded scientific figures
and wrote the first draft of the manuscript.
Conflict of Interest Statement
We thank the two anonymous reviewers for their helpful
comments and suggestions.
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