705
The Journal of Experimental Biology 215, 705-709
© 2012. Published by The Company of Biologists Ltd
doi:10.1242/jeb.065128
COMMENTARY
Physical gills prevent drowning of many wetland insects, spiders and plants
Ole Pedersen1,2,* and Timothy D. Colmer2
1
Freshwater Biological Laboratory, University of Copenhagen, Helsingørsgade 51, 3400 Hillerød, Denmark and 2School of Plant
Biology (M084), The University of Western Australia, 35 Stirling Highway, Crawley 6009, WA, Australia
*Author for correspondence ([email protected])
Accepted 16 November 2011
Summary
Insects, spiders and plants risk drowning in their wetland habitats. The slow diffusion of O2 can cause asphyxiation when
underwater, as O2 supply cannot meet respiratory demands. Some animals and plants have found a common solution to the major
challenge: how to breathe underwater with respiratory systems evolved for use in air? Hydrophobic surfaces on their bodies
possess gas films that act as a ʻphysical gillʼ to collect O2 when underwater and thus sustain respiration. In aquatic insects, this
feature/process has been termed ʻplastron respirationʼ. Here, we demonstrate the similarities in function between underwater
respiration of insect (Aphelocheirus aestivalis) plastrons and gas films on leaves of wetland plants (Phalaris arundinacea) and
also show the importance of these physical gills by the resulting changes upon their removal. The gas films provide an enlarged
gas–water interface to enhance O2 uptake underwater that is above that if only spiracles (insects) or stomata (plants) provided the
gas-phase contact with the water. Body-surface gas films contribute to the survival of many insects, spiders and plants in aquatic
and flood-prone environments.
Key words: air film, air layer, gas film, gas layer, plastron, respiration, superhydrophobic surfaces.
Introduction
The challenge of breathing underwater
Life on earth evolved in water, from which plants and animals
emerged and adopted terrestrial forms. Radiation of terrestrial
species has been prolific, and some animals and plants re-entered
the water – adopting new aquatic lifestyles. Many terrestrial
animals are also temporary visitors to the underwater world, and
wetland plants endure submergence during times of floods. These
animals and plants all risk drowning.
This Commentary presents new insights into how some
animals and plants have found a common solution to the major
challenge: how to breathe underwater with respiratory systems
evolved for use in air. We summarise various solutions used by
insects and spiders for life underwater, highlight the similarity
of one key strategy that is also used by some wetland plants and
discuss underwater insect–plant interactions related to insect O2
supply.
The strategy of particular interest involves superhydrophobic
(i.e. water-repellent) body and leaf surfaces, which underpin
‘physical gills’ on many insects, spiders and plants when
underwater. The physical gill involves retention of a gas-layer on
the superhydrophobic surfaces to provide an enlarged gas–water
interface for O2 uptake. This feature contrasts with the anatomical
gills, for example of fish, which provide a large surface area of
specialised tissue to enable exchange of O2 and CO2 between the
animal and the water. In addition to our focus here on aquatic insect
and plant eco-physiology, the superhydrophobic leaf surfaces have
also inspired development of biomimetic materials for several
applications, such as self-cleaning surfaces (paints, glass, clothes)
and attempts to reduce drag at fluid–solid interfaces (ship hulls,
pipes) and even a dome to enable humans to breathe underwater
(Koch and Barthlott, 2009; Shirtcliffe et al., 2011; Shirtcliffe et al.,
2006).
The slow diffusion of O2 in water can cause asphyxiation of insects,
spiders and plants when submerged, as O2 supply cannot meet
respiratory demands. This is why ‘virtually all adult insects and
many of their aquatic larvae, nymphs and pupae require access to
gaseous oxygen’ (Vogel, 2006). There are numerous solutions to
avoid drowning. The strategies range from frequent visits to the
surface to breathe to others that enable prolonged activities
underwater.
Snorkels enable stealth whilst obtaining air and are used by some
larvae and adult aquatic insects. There are two main snorkel types:
(1) stiff – e.g. water scorpions of the family Nepidae – and (2)
extensible – e.g. larvae of the European drone fly (Eristalis tenax).
Air tanks, carried either between the legs – e.g. the back swimmer
(Notonectidae) – or beneath the elytra of all diving beetles
(Dytiscidae) enable mobility during prolonged underwater
excursions but require surface visits to refill. Similarly, although
restricting roaming range, dive bells also enable prolonged periods
underwater. A recent study applying modern O2-sensing techniques
has improved understanding of dive bell functioning (Seymour and
Hetz, 2011). The Eurasian dive bell spider (Argyroneta aquatica)
builds a silk dome underwater attached to submerged vegetation,
which it fills with air via repeated trips to the surface. When resting,
the dive bell spider sits with its abdomen (or in some cases whole
body) within the bell so that its tracheal system accesses this store
of O2. This novel study discovered that the bell itself acts as an O2collecting device; diffusion of O2 across the bell surface can satisfy
the respiratory demand of a resting spider, even in warm (25°C)
stagnant water (Seymour and Hetz, 2011).
The function of the dive bell in O2 collection from the water results
from creation of a gas–water interface. This is analogous to physical
gills that result from gas films carried on superhydrophobic surfaces
THE JOURNAL OF EXPERIMENTAL BIOLOGY
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O. Pedersen and T. D. Colmer
500
A
Insect: Aphelocheirus aestivalis
B
400
300
O2 uptake (nmol m–2 s–1)
200
C
100
With gas film
䉱 Without gas film
0
0
250
50
100
150
200
250
300
Plant: Phalaris arundinacea
D
200
150
100
50
0
0
50
100
150
200
Dissolved O2 (µmol l–1)
250
300
Air equilibrium
at 20°C
Fig.1. A plastron acts as a physical gill and enables permanent underwater dwellers, e.g. creeping water bug (A, Aphelocheirus aestivalis) to breathe in
water (B). Some wetland plants also retain a thin gas film on their superhydrophobic leaf surfaces when submerged in water (C, Phragmites australis), and
this feature also acts as a physical gill to facilitate O2 uptake from the surrounding water (D, Phalaris arundinacea). The gas film is visible as a silvery/golden
layer (insect) or silvery layer (plant). The gas film can be removed by a few gentle brushes with 0.05% Triton X, and then rinsing, prior to submergence
(Colmer and Pedersen, 2008; Pedersen et al., 2009), and such manipulation enabled assessment of O2 uptake by the two organisms when the gas film was
removed versus when intact. The experiments were conducted at 20°C in 5ml glass cuvettes with continuous mixing (400revsmin–1); see Colmer and
Pedersen for detailed experimental procedures (Colmer and Pedersen, 2008). Duplicate measurements confirmed the responses shown. The saturation
curve for O2 uptake against external O2 concentration, of both the insect and plant with intact gas film, resembles that of respiration curves obtained for
aquatic insect larvae with haemoglobin, e.g. Chironomus sp. (Brodersen et al., 2008). Photos by Ole Pedersen.
of insects and spider bodies underwater. These gas films are easily
seen on some insects, such as the creeping water bug Aphelocheirus
astivalis (Fig.1A), for which its function as a physical gill was first
described as ‘plastron respiration’ (Thorpe and Crisp, 1947). Plastron
respiration is described in the next section. In addition to the strict
definition of plastron respiration, other insects and spiders possess
gas films on their bodies. For example, the dive bell spider also
retains a gas film on its superhydrophobic abdomen, but the gas film
area – and, consequently, gas–water interface – is insufficient to
supply enough O2 during movement (Seymour and Hetz, 2011) and
thus restricts the spider to only short hunting activities away from the
dive bell (see Fig.2).
All of the above, however, either need periodic access to the
atmosphere or replacement with fresh air at regular intervals as O2
is used in respiration or lost to the surrounding water from the air
reservoirs. Only one solution, a physical gill enabling plastron
respiration, allows some insects to remain permanently underwater.
How plastrons and compressible gas films work
A plastron acts as a collection surface on the body for inward
diffusion of O2 from water to sustain respiration and so has been
called a physical gill. A plastron is a thin film of gas trapped by
dense superhydrophobic hairs on the surface of insects (Thorpe and
Crisp, 1947). The surface area of the gas film must be large enough
for sufficient inward O2 flux to meet respiratory demand, as the gas
volume itself is too small to act as an O2 reservoir. O2 that enters
is now in the gas phase and so diffuses quickly to the tracheal
system and into the insect body. As O2 is consumed, the partial
pressure of O2 in the gas film will be lower than in the surrounding
water, resulting in an inward diffusion gradient. The dense,
specialised surface hairs, in some cases more than 6million
hairsmm–2 (Balmert et al., 2011), now play a critical second role
of maintaining the water–gas interface at a given distance from the
body and thus the volume of the gas layer, otherwise shrinkage
would occur. The increase in hydrostatic pressure that occurs with
depth (10.1kPam–1) would eventually also result in collapse of the
plastron, but ideal plastrons theoretically could be maintained down
to a depth of 400m before the tiny hairs would buckle (Vogel,
2006). However, as plastrons of the real world are far from perfect,
plastron-carrying animals are restricted to much shallower depths,
and Hinton found that, in practice, plastrons break down at
approximately 300kPa, corresponding to a depth of 30m (Hinton,
1976). It is essential that the gas film persists so that inward O2
diffusion continues to supply respiratory demands.
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707
Fig.2. The raft spider (Dolomedes fimbriatus) hunting underwater in a
shallow stream in Öland, Sweden. The abdomen of the raft spider is
superhydrophobic and retains a thin gas film underwater (visible as a
silvery layer). The gas film acts as a physical gill (see text). We have
observed that the gas film allows the spider to hunt underwater for a
minimum of 20min. In situ photo by Ole Pedersen.
Organisms with superhydrophobic surfaces, but lacking hairs to
maintain constant plastron volume, also possess a gas film when
underwater. These gas films are compressible and threatened by
severe shrinkage if the partial pressure of O2 becomes too low
(Rahn and Paganelli, 1968). Shrinkage occurs both as a
consequence of O2 consumption and also from outward diffusion
of N2. A consequence of O2 consumption is an increase in partial
pressure of N2 above external levels, such that N2 diffuses
outwards. Severe O2 depletion in the gas layer can be avoided by
having a large surface area per unit O2 demand. Thus, to be
effective, the area of gas films without underlying plastron hairs
must cover a large portion of the body [see damselfly entire body,
including wings, with gas films when underwater (Fig.3)], or a
relatively high external O2 partial pressure is required for fluxes to
sustain respiratory demands.
Two kingdoms, one solution
Leaves of many wetland plants possess gas films when submerged
(Colmer and Pedersen, 2008) – these ‘plant plastrons’ are
analogous to those of aquatic insects and spiders (Raven, 2008).
Leaf gas films occur on wetland species of particular interest,
such as the invasive weeds common reed (Phragmites australis)
(Fig.1C) and reed canary grass (Phalaris arundinacea) and the
crop rice (Oryza sativa). Leaf gas films result from retention of
air on superhydrophobic surfaces during submergence. Water
repellence results from the surface microstructure and from the
properties and nanostructure of epicuticular wax crystals
(Bhushan and Jung, 2006; Koch and Barthlott, 2009; Wagner et
al., 2003).
Superhydrophobic leaf surfaces typically lack the dense hairs
required to maintain plastron volume (described for insects in the
preceding section), and so persistence of leaf gas films is variable
amongst species (O.P. and T.D.C., personal observations) but can
last at least two weeks underwater (Colmer and Pedersen, 2008).
Leaf gas films were recently shown to enhance underwater gas
exchange by a submerged wetland plant (Spartina anglica) in a
tidal salt marsh (Winkel et al., 2011). A truly plastron-like leaf
Fig.3. Damselfly (Erythromma najas) laying eggs in the petiole of the
yellow water lily (Nuphar lutea) underwater. The petiole contains large gasfilled spaces so eggs as well as young larvae are guaranteed safe
protection and ample gaseous O2 supplied by the plant. The damselfly
typically lands on the floating leaf and then crawls over the edge of the leaf
into the water and down the petiole. The entire body, including the wings,
is superhydrophobic and retains a thin gas film underwater (visible as a
silvery layer). The gas film acts as a physical gill (see text) and enables the
damselfly to breathe underwater for as long as it takes to lay its eggs,
which can be up to 45min. Photo taken by Ole Pedersen in Lake Hampen,
Denmark, at a depth of approximately 1.2m.
surface with specialised hairs that can maintain the gas volume to
prevent water ingress was described, for the first time in the plant
kingdom, for the floating plant Salvinia molesta (Barthlott et al.,
2010). These interesting ‘eggbeater-shaped’ hairs are
superhydrophobic with the exception of the tips, a feature that also
‘pins’ the water–gas interface. Presence of this feature was
suggested to prevent formation and detachment of bubbles that
otherwise could occur when in fast-flowing waters (Barthlott et al.,
2010). This is a unique leaf surface feature, although the
ecophysiological significance could be debated, as S. molesta is a
floating plant not typically found submerged in fast-flowing waters.
However, the large gas volume trapped by these specialised
structures on the underside of the leaves would contribute
significantly to buoyancy of this floating plant.
Here, we further evaluate the similarities between the function
in underwater respiration of an insect plastron and leaf gas films.
Original data in Fig.1 compare O2 uptake by the creeping water
bug (Fig.1B) and reed canary grass (Fig.1D), including a direct
manipulation of the plastron/gas films to demonstrate the
importance of these for O2 uptake. The creeping water bug has hairs
to maintain a plastron on the ventral side. Reed canary grass forms
gas films on both leaf sides as these surfaces are superhydrophobic.
O2 uptake at various external concentrations was determined using
a micro-respiration system, with gas films intact or artificially
removed (for details, see Fig.1 caption).
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O. Pedersen and T. D. Colmer
Gas films markedly enhance underwater O2 uptake by insects
(Fig.1B) and leaves (Fig.1D). With gas films intact, O2 uptake per
unit gas-covered absorbing area (nmolm–2s–1) was approximately
400 in the creeping water bug and 200 in reed canary grass. In both
organisms, O2 uptake was independent of external concentration
down to approximately 30% of air equilibrium, below which the
inwards diffusive net O2 flux decreased (Fig.1B,D). When gas
films were removed, O2 uptake was strongly impeded, even in
water containing O2 near air equilibrium. At the lower range of
external O2, the O2 uptake rate was 3.8-fold (plant) and 3.2-fold
(insect) higher with intact gas films than when gas films had been
removed (see initial slopes of O2 uptake curves; Fig.1B,D). Thus,
for both organisms, the gas films provide an enlarged gas–water
interface for O2 uptake underwater that is above that if only
spiracles (insect) or stomata (plants) provided the gas-phase contact
with the water.
Leaf gas films also benefit photosynthesis by submerged
plants
Underwater photosynthesis enhances plant survival during complete
submergence as sugars are produced and O2 is evolved. Plants require
CO2 for photosynthesis but, when compared with leaves in air,
submerged leaves have a diminished supply of CO2, again owing to
the 104-fold slower diffusion across the aqueous boundary layers.
The CO2 concentration in the bulk medium varies greatly between
water bodies, being dependent on total inorganic carbon (CO2,
HCO3– and CO32–) and water pH; dissolved CO2 declines as pH
increases (Stumm and Morgan, 1996). Terrestrial plant leaves
possess numerous stomata, each consisting of a pore through which
gas exchange is regulated in a responsive way by guard cells on each
side. Exchange elsewhere across leaf surfaces is restricted by a waxy
cuticle. When submerged, stomata are thought to close, so CO2 must
transverse the plant cuticle, and photosynthesis is restricted in leaves
lacking gas films (Mommer and Visser, 2005). Leaf gas films
facilitate uptake of CO2 for underwater photosynthesis, in a similar
fashion to O2 entry for respiration (Colmer and Pedersen, 2008;
Pedersen et al., 2009). Moreover, leaves with gas films might also
maintain stomata open when submerged, which would by-pass the
cuticle resistance (Colmer and Pedersen, 2008). Photosynthesis, and
thus O2 production, occurs when sunlight is available and so
submerged plants only require uptake of external O2 to sustain
respiration during the night.
Animal–plant interactions
O2 within wetland plants is accessed by some insects when
underwater. Wetland plants are well known for their capacity for
internal O2 transport within their porous organs and tissues of
high gas volume (Armstrong, 1979; Colmer, 2003). The wetland
plant body provides a safe and air-filled refuge for eggs of some
aquatic insects [see the example of a damselfly laying eggs into
the petiole of the yellow water lily when underwater (Fig.3)].
Some insect larvae use needle-like breathing tubes to tap into the
hollow air-filled channels in stems and roots, e.g. Mansonia
mosquitoes (Wesenberg-Lund, 1915) and leaf beetles, Donacia
sp. (Thorpe and Crisp, 1949). More subtle, and to date only
observational, is the behaviour of some aquatic beetles that
apparently source bubbles from submerged vegetation, to
replenish their plastron [observed for the genus Elmis by Thorpe
and Crisp (Thorpe and Crisp, 1949)]. Gas taken from the surface
of submerged plants during the daytime, when photosynthesis
occurs, would be enriched in O2 (Pedersen et al., 2009) and so
such behaviour should elevate insect O2 supply.
Conclusions and implications
Internal O2 status of many insects, spiders and plants when
underwater is markedly enhanced by surface gas films acting as a
physical gill. The importance of gas films in both kingdoms, and
analogous functioning for improved gas exchange, contributes to
survival of these organisms in aquatic and flood-prone environments.
Physical gills on the body surface enable many insects, spiders
and plants to breathe underwater. This mechanism, however,
requires high-quality water with dissolved O2 near atmospheric
equilibrium; water polluted with labile organic matter has severely
decreased O2 and so is unsuitable for plastron-bearing aquatic
organisms. The sensitivity of insect plastron breathers to water
pollution has been used as an indicator of water quality (Lenat,
1993; Metcalfe-Smith, 2009). By contrast, aquatic insects that
breathe at the surface using snorkels or dive tanks can function in
low O2 waters; mass occurrence of some insects of these types can
indicate poor water quality (Lenat, 1993; Metcalfe-Smith, 2009).
In addition to sensitivity to low environmental O2, we expect that
the physical gill on insects, spiders and plants would be susceptible
to oil spills – suggested also for plants with gas films (Amstrong
et al., 2009) – and detergent pollution, as these chemicals would
interfere with the superhydrophobic surfaces required for gas film
formation and retention.
Glossary
Air equilibrium
Concentrations of dissolved gases (O2, CO2, N2) in water balance the
partial pressures of these in atmospheric air.
Biomimetics (also bionics or biomimicry)
The process in which the ideas and concepts developed by studies of
nature are taken and implemented into technology (Koch et al., 2009).
Cuticle
(zool.) An outer protective layer of material produced by the epidermal
cells that covers the body of many invertebrates; (bot.) a layer of waxy
material on the outer wall of epidermal cells in many plants, making them
fairly impermeable to water (Lawrence, 1993).
Diffusion
The free passage of molecules, ions, etc. from a region of high
concentration to a region of low concentration (Lawrence, 1993). The
process determines the net flux across diffusive boundary layers and is
described by Fick’s 1st law of diffusion: J–D(⌬C/X), where J is the flux
(molm–2s–1), D is the diffusivity (m2s–1) of the substance in the particular
medium, and ⌬C is the concentration difference (molm–3) between two
positions of distance X (m). Taking O2 as an example, the diffusivity is
104-fold higher in air compared with in water (e.g. at 20°C, 2.03⫻10–5 in
air, 2.10⫻10–9 in water). Diffusivity increases with temperature (e.g. for
O2 in water 0.99⫻10–9 at 0°C to 3.16⫻10–9 at 40°C) [for diffusivisities of
O2 at various temperatures and salinities, see Ramsing and Gundersen
(Ramsing and Gundersen, 2011)]. Some applications of the Fick equation
use partial pressure differences rather than concentration differences
(Moyes and Schulte, 2008).
Elytra
The forewings of beetles, which are hard and stiff and are not flapped in
flight but serve, at rest, as a protective covering for the membranous
hindwings (Lawrence, 1993).
Gas solubility
The solubility of gases in water is strongly temperature dependent;
concentrations in warm water are lower than in cold water. The response
to increasing water temperature is stronger for CO2 (77.6 and
23.9mmoll–1 at 0 and 40°C, respectively, for pure CO2 at 101.3kPa) than
for O2 (2.2 and 1.0mmoll–1 at 0 and 40°C, respectively, for pure O2 at
101.3kPa) (Weiss, 1974).
Haemoglobin
O2-carrying haem protein; the principal O2 carrier in vertebrate blood
(Lawrence, 1993).
THE JOURNAL OF EXPERIMENTAL BIOLOGY
Physical gills in animals and plants
709
References
Hydrophobic
Water-repelling or repelled by water, as non-polar groups on lipids,
proteins, etc., which tend to aggregate, excluding water from between
them (Lawrence, 1993).
Partial pressure
In a mixture of gases, each gas has a partial pressure that is the pressure
that the gas would have if it alone occupied the volume. The total pressure
of a gas mixture is the sum of the partial pressures of each individual gas
in the mixture (Moyes and Schulte, 2008). The partial pressure of a gas
dissolved in a liquid is defined as the partial pressure that the gas would
exert if the gas phase were in equilibrium with the liquid.
Petiole
(bot.) The stalk of a leaf; (zool.) the slender stalk connecting the thorax
and abdomen in certain insects (Lawrence, 1993).
Photosynthesis
The synthesis of carbohydrate in a chloroplast from CO2 as a carbon
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Structural adaptation, common among some types of aquatic insects,
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A respiration organ consisting of an air space possessing (i) a large surface
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Respiration
Any or all of the processes used by organisms to generate metabolically
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Spiracle
Hole in the sides of the thoracic and abdominal segments of insects, and
of myriapods, through which the tracheal respiratory system connects with
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Stomata
Small openings in the epidermis of aerial parts of plants through which
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Trachea
One of the air-filled tubules of the respiratory system, which opens to the
exterior through openings (spiracles) in the sides of the thorax and
abdomen of insects (Lawrence, 1993).
Acknowledgements
We thank Dr Dean Jacobsen and two anonymous referees for constructive
feedback on the manuscript.
Funding
This study was funded by the Centre for Lake Restoration, a Villum Kann
Rasmussen Centre of Excellence and the Danish Council for Independent
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