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Reasons for the presence or absence of convective
(pressurized) ventilation in the genus Equisetum
Jean Armstrong and William Armstrong
Department of Biological Sciences, University of Hull, Kingston upon Hull, HU6 7RX, UK and School of Plant Biology, Faculty of Natural and
Agricultural Sciences, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia
Summary
Author for correspondence:
Jean Armstrong
Tel: +44 1964 550135
Email: j.armstrong@hull.ac.uk
Received: 19 August 2010
Accepted: 24 September 2010
New Phytologist (2011) 190: 387–397
doi: 10.1111/j.1469-8137.2010.03539.x
Key words: aerenchyma, anatomy,
Equisetum spp., gas flow resistance,
humidity-induced convection, intercalary
meristem, oxygen, wetland.
• The very high rates of convective ventilation reported recently in Equisetum
telmateia (up to 120 cm3 min)1; internal wind speed, 10 cm s)1) prompted this
study of a further eight species for the presence or absence of convection and the
possible reasons for this.
• Convection rates were examined in relation to anatomical pathways, internal
resistance to applied pressurized gas flow and stomata.
• Only species with interconnecting cortical aerenchyma in branches (when present), shoots and rhizomes induced convection. Rapid humidity-induced convection
(HIC) occurred in E. palustre (up to 13 cm3 min)1), with slower rates in E. ·
schaffneri and E. ramosissimum (£ 6 and 3 cm3 min)1, respectively). Excised
shoots of E. hyemale and E. fluviatile showed the potential for HIC (£ 0.5 and
0.15 cm3 min)1, respectively), but not into the rhizomes. High rates were linked to
low internal gas flow resistance. No convection was detected in E. scirpoides,
E. sylvaticum or E. arvense due to the extremely high resistance to pressure flow,
for example, from intercalary meristems and, in the last two, to nonaerenchymatous branches.
• Of the nine Equisetum species studied so far, four showed through-flow
convection; the other species must rely solely on diffusion for underground aeration in wet soils.
Introduction
For some time, convective (pressurized) ventilation through
the internal gas space system has been known to occur in
certain aquatic macrophytes: for example, in water-lilies
(Dacey, 1980; Grosse, 1996), the common reed, Phragmites
australis (Armstrong & Armstrong, 1990; Armstrong et al.,
1992; Brix et al., 1992), Eleocharis sphacelata (Sorrell &
Boon, 1994) and Typha spp. (Bendix et al., 1994). More
recently, in a nonflowering species, the great horsetail,
Equisetum telmateia, very high rates of convection have been
found; these possibly also occurred in extinct tree horsetails, the Calamites, of the Carboniferous (Armstrong &
Armstrong, 2009).
Convections, or ‘internal winds’, generated across stomata
(or other micropores) by humidity-induced diffusion (HID)
and sometimes also by thermal transpiration, which represent types of molecular pump (Armstrong & Armstrong,
1994; Armstrong et al., 1996a,b), pass through shoot and
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rhizome aerenchyma and vent via shoot parts of small gas
flow resistance, for example, senesced shoots or stubble.
Under warm conditions and low relative humidity (RH),
rates of convection for leaves of the giant water-lily Victoria
amazonica (Grosse et al., 1991) and for single shoots of
P. australis (J. Armstrong et al., 1996) and E. telmateia
(Armstrong & Armstrong, 2009) can be as high as 83, 17
and 120 cm3 min)1, respectively. In E. telmateia, the ‘internal wind’ through the aerenchyma may reach 10 cm s)1.
These convection rates are those for excised shoots; depending on resistances in the gas flow pathway, they are lowered
by very variable degrees when connected to the rhizome; for
example, in E. telmateia, rates can be reduced by 60%.
Many emergent macrophytes have roots and rhizomes
growing in waterlogged anoxic soils that are nitrate deficient
and rich in phytotoxins, such as iron (Fe2+), manganese
(Mn2+), sulphides and organic acids. Adequate supplies of
atmospheric oxygen to the underground parts and to the soil
via the roots are essential for the supply of respiratory O2 to
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the roots and rhizomes and for the oxidation of phytotoxins
in rhizosphere regions around roots (Armstrong & Drew,
2002; Colmer, 2003). The advantage to emergent aquatic
macrophytes of convective over the more usual diffusive
ventilation is that convective flows can, over long distances,
supply oxygen for rhizome respiration (Armstrong &
Armstrong, 1990; Armstrong et al., 1992) and vent waste
gases, such as CO2 (Brix et al., 1996), more effectively than
diffusion. In addition, by conveying ‘fresh air’ to root–rhizome junctions, convection greatly increases O2 diffusion to
roots and radial O2 loss to the rhizosphere (Armstrong &
Armstrong, 1990; Armstrong et al., 1992, 1996), where it
can oxidize phytotoxins (Begg et al., 1994; Pedersen et al.,
2004) and induce nitrification (Kirk & Kronzucker, 2005).
Other important advantages of convective aeration are that
greater numbers of roots can be supported and the penetration depth for rhizome and root growth can be greatly
increased (Vretare-Strand, 2002; Sorrell & Hawes, 2010);
convection also increases oxygen supplies to rhizome tips
and surrounding phyllospheres (Armstrong et al., 2006).
Moreover, the purging properties of convective flows
through rhizomes should enhance the removal of ethylene
from roots and help to avoid its accumulation to growthinhibiting levels (Visser et al., 1997). All these effects
should enhance the competitive advantage of such plants
(Vretare-Strand, 2002; Sorrell & Hawes, 2010). It has been
reported that the rhizomes of E. telmateia can penetrate to
4 m depth in wet soil (Page, 1997).
The Equisetales is an ancient group of nonflowering
vascular plants probably dating back 250 million years to
the Upper Carboniferous era (Bell & Hemsley, 2000) but,
apart from Barber’s (1961) report on E. fluviatile, the aeration system of these plants has been given little attention in
the literature. This article explores the pathways of aeration
in eight extant species of Equisetum, the possibility that convective flows take place and the reasons for the occurrence
or absence of convections. The investigation was conducted
in relation to the mechanism of convection, anatomical
pathways, stomata and internal resistance to applied pressurized gas flow.
Materials and Methods
Plant material
The sources of Equisetum were as follows: E. · schaffneri
Milde, one of the ‘giant horsetails’ (Royal Botanic Gardens,
Kew, UK); E. sylvaticum L. (near Finchdale Priory, Co.
Durham, UK); E. fluviatile L. (Weedley Springs, South
Cave, East Yorkshire, UK); E. ramosissimum Desf.
(University of Utrecht Botanic Gardens, the Netherlands
and Mazzolla, Tuscany, Italy); E. hyemale L., E. scirpoides
Michaux, E. palustre L. and E. arvense L. (Botanic Gardens,
University of Hull, UK); and E. telmateia Ehrh. used for
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comparisons (Warter Farms Estate, Pocklington, East
Yorkshire, UK). Plants were collected between May and
September 2009 and 2010; freshly excised shoots were used
for field experiments; for laboratory experiments and anatomy, plants were transported within Perspex tubes with the
bases in water and used within a few hours.
Convection rates
Rates of convective free flow from whole excised shoots
were measured by connecting the basal end by rubber tubing sealed on with silicon rubber to either a digital or soap
film flow meter. Convection into the underground rhizome
was detected by inserting a flow meter in series between the
shoot base and its stubble. Appropriate corrections to flow
measurements were made to negate the effects of flow meter
resistance. Static pressure (DPs) the maximum pressure
developed with the plant connected to the pressure
transducer only and the convective flow blocked, was measured by means of a digital pressure transducer (Radio
Spares, Corby, Northamptonshire, UK); it is the pressure at
which Poisseuille outflow to the atmosphere through stomata is balanced by the inflow of gases and the effect of
internal humidification within the plant. RH and temperature were measured using a combined probe (Vaisala,
Malmo, Sweden), the photosynthetic photon flux rate using
a portable light meter (Li-Cor, Lincoln, NE, USA) and
stem diameters by means of digital callipers.
Gas space continuity: anatomy
The continuity of gas spaces within the plant was investigated anatomically using an Olympus BX40 photomicroscope on fresh material from transverse sections of aerial
branches (where present) and stem and rhizome internodes
and nodes.
Gas space continuity: resistances to applied
pressurized through-flow and convection
Gas flow resistances and flows were measured at pressures
realizable by HID: £ 1000 Pa on excised stems or parts of
stems, cut at each end and with aerenchyma channels
and ⁄ or pith cavity variously sealed with silicon rubber, as
described in Armstrong & Armstrong (2009). In some
cases, stepwise excision, by successive node and internode,
was used to obtain details on the distribution and magnitude of pressure flow resistance. Pressure flow resistances
(RP: Pa s cm)3) were calculated from the relationship,
RP = F ⁄ DP, where F (flow rate) is in units of cm3 s)1.
The cut ends of convecting shoots (sometimes with
rhizomes) were immersed just under the water surface to
ascertain the pathway of convection from the pattern of
bubbling.
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Results and Discussion
To present a complete picture, some relevant previous
results for E. telmateia have been included.
Convection rates
Significant convective flow rates were found for excised
stems in E. palustre (up to 13 cm3 min)1), E. · schaffneri
(£ 6 cm3 min)1) and E. ramosissimum (£ 2–3 cm3 min)1)
(Table 1). These were measured at comparatively low RH
(c. 40–50%), T = 20–24C and photosynthetic photon flux
rate (700–1700 lmol m)2 s)1); at 30% RH and higher
temperatures, values could have been doubled. For example,
a rise in temperature from 24C to 32C alone almost doubles the saturated water vapour pressure (3000–4800 kPa),
and hence the potential for convection, whereas a decrease in
external humidity from just 40% to 30% RH can increase
the internal pressurization by a further 20% (Armstrong &
Armstrong, 2009). Convection rates were directly related to
stem height and total branch length (e.g. for E. palustre,
Fig. 1a,b); the static pressure DPs (Fig. 1c), an indicator of
convective flow potential, was inversely related to RH, and
correlated with previous results for E. telmateia (Armstrong
& Armstrong, 2009). We conclude that in these species also
the flows are induced by humidity differentials.
Flows were extremely low in E. fluviatile (£ 0.15
cm3 min)1). In E. hyemale, there was the potential for flow
Table 1 Examples of pressure flow resistance of gas space and convective flow rates for Equisetum spp.
Pressure flow resistance of lower stem gas
space
Subgenera
Species
Subgenus Hippochaete
E. scirpoides
E. ramosissimum
E. · schaffneri
E. hyemale
Subgenus Equisetum
Section Subvernalia
Section Nova
E. sylvaticum
E. fluviatile
E. arvense
Section Palustria
E. palustre
E. telmateia
Internodal aerenchyma
(Pa s cm)3 mm)1)
Nodes
(Pa s cm)3)
Convection
rate (cm)3 min)1)
NA
c. 1–2
c. 1–2
unless intercalary
meristem present
10–15
2
¥
NA
¥
10–25k
200–500
1
15–19k
0
£ 3.0
£ 6.0
130–150k
1
£ 1M
¥
3
0
NA
c. 1–2
2
¥
c. 1–2
<1
NA
¥
£ 0.15
0
70–300
4–50
£ 13
£ 120
0.5
12
10
8
6
4
2
0
0
10
20
30
40
50
60
Shoot length (cm)
(b)
14
12
(c)
Static pressure (Pa)
14
Convective flow rate
(cm3 min–1)
(a)
Convective flow rate
(cm3 min–1)
NA, not available.
1
, Radial channels.
2
, Including intercalary meristem.
3
, Potential flow from individual internodes only.
10
8
6
4
2
0
0
350
300
250
200
150
100
50
200
400
600
800
Total branch length
+ terminal segment (cm)
0
0
20
40
60
80
100
Chamber humidity (% RH)
Fig. 1 Equisetum palustre: rates of convective flow (free flow from excised shoots) in relation to shoot length (a) and total branch length (b).
(c) Typical example of static pressures of isolated branched node vs external (chamber) relative humidity (RH).
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(a)
0.6
Convective flow rate
(cm3 min–1)
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0.5
As with E. telmateia, convective flows passed into the rhizomes in E. palustre, E. ramosissimum and E. · schaffneri.
There was no evidence of gaseous through-flow into the rhizome system in E. hyemale or E. fluviatile, so we conclude
that, although there is the potential for humidity-induced
convection (HIC) generated by internodes, it does not take
place in these species.
0.4
0.3
0.2
0.1
0.0
Base N IN N IN N IN N IN N IN N IN N IN N IN
1 1 2 2 3 3 4 4 5 5 6 6 7 7 8 8
Apex
Gas space continuity from anatomy
Node/internode number present at base
(b)
Stomata Equisetum palustre resembles E. telmateia in that
the branch stomata bear, on the external surface of the subsidiary cells, close-fitting elongated pilulae (papillae) which
overarch the stomatal pore (Fig. 3a,b; Table 2) (Page,
1972; Armstrong & Armstrong, 2009). In E. sylvaticum
and E. arvense, these pilulae are short, sparse and not overarching; stomatal pilulae are absent in E. ramosissimum
(Fig. 3d), E. · schaffneri (Fig. 3e), E. hyemale and E. fluviatile
(Page, 1972; Table 2).
Convective flow rate
(cm3 min–1)
0.5
0.4
0.3
0.2
0.1
0.0
0
2
4
6
8
10
12
14
16
18
20
22
Individual internode surface area (cm2)
Fig. 2 Equisetum hyemale: (a) convective flow rates (free flow from
excised shoots) for stepwise removal, from base, of single
node + internodal segments of the same shoot (N, node; IN,
internode); (b) convective flow rates from two typical shoots vs
surface areas of basal internodes obtained from stepwise shortening
of stems (shoot 1, open circles; shoot 2, closed circles). In this
species, convective flow is from the basal internode of the stem
only; nodes are impermeable to gas flow.
from each internode (£ 0.5 cm3 min)1), but flow between
internodes was blocked by the intercalary meristems (Fig. 2a).
In addition, the flow rate was proportional to the surface area
of the connected internode (Fig. 2b). No convective flows
were detected in E. scirpoides, E. sylvaticum or E. arvense.
Branches Apart from the unbranched E. hyemale and
E. scirpoides (Fig. 5f,i) and the inconsistently branched
E. ramosissimum (Fig. 4c), stems of all the other species
investigated possess a whorl of branches at each node,
except for the basal ones (Fig. 4a,e,g,i,l,S3). Only the
branches of E. palustre, E. · schaffneri and E. ramosissimum
resemble those of E. telmateia in possessing aerenchyma
(Fig. 4b,h,d, Table 2) directly interconnecting between
the internodes and nodes; the branches of E. sylvaticum,
E. fluviatile and E. arvense generally have no aerenchyma
channels (Fig. 4f,j,k,m), but those of E. arvense sometimes
contain aerenchyma in proximal internodes. Pith cavities
are present in the branches of all species examined, except
for E. sylvaticum and E. arvense. Prominent substomatal
Table 2 Aeration anatomy and branch morphology in Equisetum spp.
Stem endodermis
Aerenchyma (vallecular canals)
Species
Stomatal
pilulae
E.
E.
E.
E.
E.
E.
E.
E.
E.
)
)
)
)
Sparse short
Sparse short
Sparse short
Close long
Close long
scirpoides
ramosissimum
· schaffneri
hyemale
sylvaticum
fluviatile
arvense
palustre
telmateia
Branch sections
(no. sides)
Branch
internodes
6
8
+
+
4
4
2
Cruciform
5 or 6
8
)
)
3
)
+
+
Stem
internodes
Stem
nodes
Stem nodal
radial channels
Stem
internodes
Stem
nodes
)
+
+
+
+
+ lso
+
+
+
)
+
+
+disc.
+disc.
+disc. lso
+disc.
+
+
)
+
+
1
)
)
1
) lso
)
)
)
Single circum.
Double
Double
Double
Single circum.
Single vb
Single circum.
Single circum.
Single circum.
Single circum.
Single vb
Single vb
Single vb
Single circum.
Single vb
Single circum.
Single circum.
Single circum.
+, Present; ), absent; circum., circumferential, encompassing all the vascular bundles; disc., discontinuous because of intercalary meristem; lso,
lower stem only; vb, around each vascular bundle.
1
, Radial gas spaces for diffusion present.
2
, Apart from basal internode which is hexagonal.
3
, Apart from proximal internode which may possess aerenchyma.
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E. telmateia
(a)
E. ramosissimum
(d)
E. palustre
(b)
E. x schaffneri
(e)
(c)
Fig. 3 Branch stomata in species of Equisetum that show convective
flow. (a, b, d) Scanning electron micrographs of outer surfaces of
stomata of E. telmateia, E. palustre and E. ramosissimum,
respectively. Note pilulae in (a, b). (c) Transverse section of branch
of E. palustre showing substomatal cavities. (e) Outer surface of
stoma of E. · schaffneri by light microscopy. Bars: (a, b, d, e)
10 lm; (c) 50 lm. (a, b, d) After Page (1972); reproduced with
permission of the New Phytologist Trust.
cavities are visible in all branches (e.g. Fig. 3c) and in the
stems of E. scirpoides and E. hyemale; these cavities connect
with aerenchyma channels, when present, via intercellular
spaces.
Stems Apart from E. scirpoides, the stems of all species possess
a central pith cavity (Fig. 5d,g,k,o,r,t) traversed by a diaphragm
at each node (Fig. 5b,h,m,p). Diaphragms may be quite
porous (E. · schaffneri: Fig. S3, E. fluviatile and
E. ramosissimum) or relatively lacking in gas space
(E. telmateia, E. palustre and E. arvense). In all the species
studied here, apart from E. scirpoides and E. fluviatile, cortical aerenchyma channels (vallecular canals) are present in all
stem internodes (Fig. 5a,g,k,o,r,t, Table 2). We found
them to be absent in E. scirpoides (Fig. 5j); however,
Johnson (1933) reported their presence. In E. fluviatile, aerenchyma channels are present only in the lower unbranched
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half of the stem (Fig. 5d) and absent in the upper branched
part (Fig. 5c). Within the genus, aerenchyma channel discontinuity in stems can be a result of nonaerenchymatous
blockages in the region of the intercalary meristem level
with the top edges of the leaf sheath, as in E. fluviatile,
E. · schaffneri, E. arvense and E. sylvaticum (Fig. 5e,l,s,u,
Supporting Information, Fig. S1). In E. hyemale (Fig. 5h),
there can also be a blockage close to the node. However,
in E. · schaffneri (lower part of stem), E. palustre and
E. ramosissimum (Fig. 5b,n,p, Table 2), successive internodal cortical aerenchyma channels connect directly across
the nodes; similar connections have also been found previously in E. telmateia (Armstrong & Armstrong, 2009). In
E. · schaffneri and E. ramosissimum stems, near the lower
edge of the pith diaphragm, there are radial channels
of sufficient porosity for pressure flow between cortical
aerenchyma channels and the pith cavity (Fig. 5m,q, S3,
Table 2); these are similar to the radial channels of Phragmites
(Armstrong & Armstrong, 1988) and the infranodal canals
of the extinct Calamites (Williamson, 1871; Boureau, 1964;
Armstrong & Armstrong, 2009). Examples of internodal
anatomy for some of these species can also be found in
Brune et al. (2008).
It was interesting to note the form of the endodermises in
the various species. It seems certain that the Casparian
bands will prevent apoplastic gas space connection, and this
is apparent from microscopy as well as applied pressurized
through-flow examination. E. fluviatile has an endodermis
around each vascular bundle; elsewhere internodal endodermises are circumferential (around all the vascular
bundles collectively), with either an internal and external
endodermis, as in E. ramosissimum, E. · schaffneri and
E. hyemale (Fig. S2), or single external as in E. sylvaticum,
E. arvense, E. palustre and E. telmateia (Table 2). These
endodermises should prevent internodal apoplastic gas connection between aerenchyma and the pith. However, at the
nodes in E. ramosissimum, E. · schaffneri and E. hyemale,
the two endodermises are lost and each vascular bundle is
surrounded by its own endodermis, allowing apoplastic gas
space connections between aerenchyma and pith cavity,
which are visible microscopically; in the first two species,
there are radial channels of low porosity enabling some
convective flow in this direction. However, in E. arvense,
E. palustre and E. telmateia, there are no radial gas connections, the nodal endodermises are circumferential and
convection is via the aerenchyma channels only in the last
two species.
Rhizomes The rhizomes of E. arvense, E. fluviatile, E. hyemale,
E. ramosissimum and E. · schaffneri resembled stems in
containing a pith cavity and surrounding cortical aerenchyma channels; the rhizomes of the other species
contained only aerenchyma channels.
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(a)
E. palustre
(b)
E. x schaffneri
(g)
(h)
E. ramosissimum
(i)
E. fluviatile
(j)
(c)
(d)
(k)
(l)
(e)
E. sylvaticum
(f)
E. arvense
(m)
Fig. 4 Habits and branch anatomy for species of Equisetum. (a, c, e, g, i, l) Habit; bars, 5 cm. (b, d, f, h, j, k, m) Transverse sections of branch
internodes; bars, 200 lm.
Gas space continuity from applied pressure flows and
convection
As in E. telmateia, it was possible to blow gas through stem
aerenchyma channels of successive internodes and nodes in
E. palustre and E. ramosissimum, and through the lower
parts of the stem in E. · schaffneri; this was consistent with
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the nodal aerenchyma connections described above. There
was more resistance to flow through the aerenchyma channels of the nodes than the internodal cortex in E. telmateia,
and E. palustre (Fig. 6), E x schaffneri and E. ramosissimum
(Table 1) because of a narrowing of the channels at the nodes
(Fig. 5a,b,k,m,o,p). Gas could only be blown through aerenchyma of excised stem internodes, but not through that of
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E. x schaffneri
E. palustre
(a)
(b)
(k)
(l)
(m)
(n)
E. fluviatile
E. ramosissimum
(c)
(o)
(p)
(q)
(d)
(e)
(f)
E. hyemale
E. arvense
(g)
(r)
(s)
(h)
E. scirpoides
(i)
(j)
E. sylvaticum
(t)
(u)
Fig. 5 Stem aeration anatomy and habits for species of Equisetum. (a, c–e, g, j–l, o, r–u) Transverse sections of stem internodes: from upper
branched part of stem (c), lower unbranched part of stem (d, e), near intercalary meristem at top of leaf sheath (e, l, s, u), and mid-internode
(a, d, g, j, k, o, r, t). (b, h, m, n, p, q) Transverse sections of stem nodes, that is, near diaphragms, and insertion of branches when present. (f,
i) Habits. Bars: (a–e, g, h, j–u) 400 lm; (f, i) 5 cm. Arrows show position of radial connections in (m) and (q).
successive internodes and nodes, in E. arvense, E. hyemale
and E. fluviatile, because of virtually infinite resistance to
through-flow through the intercalary meristem (e.g. for
E. arvense, Fig. 7), and in E. hyemale because of a lack of
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aerenchyma in the nodes. The pith cavities of E. fluviatile,
E. ramosissimum and E. · schaffneri were permeable to gas
flow, but not those of E. palustre, E. telmateia or E. arvense.
As found previously for E. telmateia, aerenchyma channels of
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(a) 200
(c)
IN
160
4000
N
140
IN
120
3500
100
N
80
IN
60
40
N
20
IN
0
0
20
40
60
80 100 120 140 160
Distance along segment (mm)
(b) 300
Accumulated pressure-flow
resistance (Pa s cm–3 s–1)
IN
250
200
Accumulated pressure-flow resistance (Pa s cm–3)
Accumulated pressure-flow
resistance (Pa s cm–3 s–1)
180
3000
2500
2000
1500
1000
500
150
N
0
100
0
50
0
IN
0
10
2
Base
20
30
40
50
60
4
6
Node
8
10
Apex
70
Distance from basal end (mm)
Fig. 6 Typical examples of accumulated resistances to applied gaseous pressure flow in stems ⁄ stem segments as detected from: (a) sequential
removal of single nodes (N) and intermodal (IN) material in Equisetum telmateia stem; (b) sequential shortening of a single node with part of
internode on each side for E. palustre; (c) sequential removal of individual node + internodal segments in E. palustre (compare with Fig. 7).
branches, stems and rhizomes were interconnected in
E. palustre, E. · schaffneri and E. ramosissimum, and pith
cavities of stems and rhizomes in E. · schaffneri and
E. ramosissimum.
When the cut ends of excised shoots were just immersed
in water, bubbles were observed from the aerenchyma
channels only in E. palustre and E. telmateia, and from
both aerenchyma and pith cavity in E. · schaffneri and
E. ramosissimum, giving some indication of the convective
flow pathways. The same applied when parts of the rhizomes
were attached.
Final comments
The type of convection found so far among the Equiseta
appears to be induced by humidity differentials (Fig. 1c;
Armstrong & Armstrong, 2009). This relies on HID, a kind
of ‘molecular-pump’ involving the inward diffusion of O2
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and N2 through narrow (< 1 lm) stomatal pores highly
resistant to pressurized Poiseuille backflow. Details on the
mechanism are given in Armstrong & Armstrong (1994)
and Armstrong et al. (1996a,b). In summary, diffusion gradients are induced by humidification within the plant,
which reduces O2 and N2 concentrations to below atmospheric levels. The inwardly diffusing gases, together with
water vapour continually produced from substomatal cells,
cause a pressurization which drives convective gas flows
(‘internal winds’) along the path of least resistance through
stem and rhizome with venting through older, more porous
parts of the plant (Dacey, 1980; Armstrong et al., 1996).
HIC is powered by the latent heat of evaporation, to maintain the humidity of the gas spaces, and is most rapid under
warm, dry (low RH), sunny conditions (Armstrong et al.,
1996; Brix et al., 1996; Steinberg, 1996). Under conditions
of 100% RH and at night, rates of HIC are normally very
low or zero, so that the plants must then rely on diffusive
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Research
100
>106
Pa s cm–3
at 58 mm
Segment pressure-flow resistance (Pa s cm–3)
90
80
70
60
50
40
30
20
10
0
0 10 20 30 40 50 60 70 80
Distance along segment (mm)
Fig. 7 Typical example of accumulated resistances to applied
gaseous pressure flow by sequential removal of individual
node + internodal segments in Equisetum arvense stem (compare
with Fig. 6b).
ventilation. Living shoots are necessary for HIC; for species
which die back, this only occurs during the growing season.
The pathways of convection vary between species and are
summarized in Fig. 8.
In E. telmateia, E. palustre, E. · schaffneri and E. ramosissimum, features that appear to correlate with the ability to
induce significant convective flows are the continuity of the
aerenchymatous gas space between shoot and rhizome
(Figs 3, 4) and the internal resistance to gas flow, which
can be overcome by pressures generated by HIC (Fig. 6;
Tables 1,2). Rapid convection in E. telmateia and E. palustre
is linked to the low resistances to gas flow, numerous aerenchymatous branches which provide large stomatal areas and,
possibly, rows of closely interlocking stomatal pilulae (Fig. 3a,b)
close to the optimal pore width (0.2–0.3 lm), helping to
curtail backflow. In E. · schaffneri and E. ramosissimum,
where convection rates are slower (£ 6 and 3 cm3 min)1,
respectively), branches are sparser (Fig. 4c,g) and stomatal
pilulae are absent (Fig. 3d, e). However, relative to the sizes
of the plants, convection rates are greater in the latter.
Potential flow rates in E. hyemale and E. fluviatile are very
slow and of little significance because they cannot be transmitted to the rhizomes. Blockages in the stem cortical aerenchyma are not bypassed in E. hyemale and E. fluviatile,
whereas they are bypassed to some extent via radial channels
into the pith cavity in E. · schaffneri and E. ramosissimum.
As mentioned in the Introduction, convective ventilation
has been considered to be advantageous for a number of
wetland plants and, apart from E. arvense, the species studied grow in damp to wet habitats (Clapham et al., 1952;
Husby, 2003). Vretare-Strand (2002) concluded that species with pressurized ventilation have a competitive advantage in deep water, resulting in long-term competitive
exclusion of species lacking pressurized ventilation, and that
this will affect species’ zonation patterns along water depth
gradients, with a more pronounced effect in substrates with
low redox potentials. Similarly, Sorrell & Hawes (2010)
concluded that the development of convective flow appears
to be essential for the dominance of helophyte species in
> 0.5 m depth, especially under eutrophic conditions,
although exposure, sediment characteristics and light attenuation frequently constrain them to a shallower depth than
their flow capacity permits. We suggest that, also in
Equisetum, HIC may help roots and rhizomes to grow to
greater depths and extent, and contribute to an increased
competitive advantage.
Page (1997) reported that rhizomes of E. telmateia can
penetrate to 4 m depth in wet soil, but E. fluviatile is the
only Equisetum species that we examined which commonly
grows in 30–60 cm depth of standing water, whereas
E. hyemale can also grow partly submerged; surprisingly,
these species have no effective convection. However, they
appear to be very well adapted for diffusive ventilation
E. telmateia and E. palustre
Branch
stomata
Substomatal
cavities
Branch
aerenchyma
E. ramosissimum and E. x schaffneri
Branch
Branch
Substomata
aerenchyma
stomatal
cavities
Stem
nodal
aerenchyma
Stem
nodal
aerenchyma
Via radial
channels
†
Stem
internodal
aerenchyma
Rhizome
aerenchyma
Stem
internodal
aerenchyma
Rhizome
aerenchyma
Stem
pith cavity
Venting via
stubble or
damaged shoots
†
†
Rhizome
pith cavity
Venting via
stubble or
damaged shoots
Fig. 8 Pathways of convective flow in some species of Equisetum. †Convective flow will enhance O2 diffusion into (i) roots and radial oxygen
loss to the rhizospheres and (ii) into rhizome apices and ROL to the phyllospheres.
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(Barber, 1961; Hyvonen et al., 1998): they possess thinwalled stems (Fig. 5d,g), with probably low overall respiration
rates, and a wide pith cavity in stem and rhizome with relatively porous diaphragms.
Equisetum sylvaticum, E. scirpoides and E. arvense lack
continuity of aerenchymatous connections between branches
(where present), stem and rhizome (Figs 4, 5, S1); the last
two species show infinite resistance to applied pressurized
gas flow through the stem (Table 1) and it is therefore not
surprising that these three species are nonconvecting. There
is clearly great diversity within the living Equiseta in terms
of their ability to induce convective ventilation, and their
aeration systems are rather complex; we tend to agree with
Milde (1867) who declared that, ‘Sine examine microscopico nulla scientia Equisetorum!’ – ‘Without microscopic investigation, (there can be) no knowledge of the
Equiseta!’
Acknowledgements
We thank Mr Victor Swetez (University of Hull, UK) for
horticultural assistance, Mr David Cook (Royal Botanic
Gardens, Kew, UK) for allowing us to experiment on
E. · schaffneri, Dr B.P. van de Riet (University of Utrecht,
the Netherlands) for supplying E. ramosissimum and Mr
C.M. Redfern (Warter Priory Farms, East Yorkshire, UK)
for permitting access to the stands of Equisetum telmateia.
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Supporting Information
Additional supporting information may be found in the
online version of this article.
Research
below the intercalary meristem and their lost continuity
across the meristem.
Fig. S2 Equisetum hyemale: transverse sections of internode
showing an internal and external endodermis with Casparian
bands.
Fig. S3 Equisetum · schaffneri: slides of habit and higher
definition slides of stem anatomy showing gas transport
features.
Please note: Wiley-Blackwell are not responsible for the
content or functionality of any supporting information
supplied by the authors. Any queries (other than missing
material) should be directed to the New Phytologist Central
Office.
Fig. S1 Equisetum arvense: transverse sections of stem internode showing aerenchyma (vallecular canals) above and
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