Transport of Carbon and Phosphorus Compounds about Sphagnum
Author(s): H. Rydin and R. S. Clymo
Reviewed work(s):
Source: Proceedings of the Royal Society of London. Series B, Biological Sciences, Vol. 237, No.
1286 (Jun. 22, 1989), pp. 63-84
Published by: The Royal Society
Stable URL: http://www.jstor.org/stable/2410553 .
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Proc. R. Soc. Lond. B 237, 63-84 (1989)
Printedin GreatBritain
Transportof carbon and phosphoruscompounds
about Sphagnum
BY H. RYDINt
AND R. S. CLYMO
School ofBiological Sciences, Queen Mary College,London El 4NS, U.K.
(Communicatedby G. E. Fogg, F.R.S. - Received 8 November1988)
[Plates 1 and 2]
The bog mosses, Sphagnum, lack any obvious anatomical specialization
inside the stem but have a well-developedsystemof water conductionin
capillary spaces among pendent branches around the stem. It has hitherto been assumed that this was the main route for solute transfertoo.
We describe experimentsshowingthat thereis rapid and quantitatively
importanttransportwithin the stems.
The tracers 32P and 14Cwere supplied to S. recurvum.When applied
below the top ofthe plant they moved to the apex whetherexternalmass
flow was upward or downward. Autoradiographs showed high concentration of tracers in the stem. Steaming the stem above and below the
site of application prevented tracer movement.
An experimentlasting fourweeks on S. papillosum showed that after
14C labelling almost all that part of the alcohol-soluble fraction that
moved did so fromolder parts to the apex, with verylittletransferto the
insoluble fraction,to neighbours,or into the gas phase. For the soluble
fractionin the capitulum, the conductance for14Cfrombelow was about
the same as that of its loss in respiration. The conductance to the
insoluble fractionwas about twice as great, and to neighboursabout half
as much.
A longer experimentshowed that predominatelyacropetal transport
continued forat least 22 weeks in fivespecies. By that time about 25 %
of the remaining14Clabel was incorporatedin the new tissues.
The stem of S. recurvumcontains a central mass of parenchyma20-50
cells across. The end walls of the parenchyma cells have perforations
approximately 100 nm across at a densityof 7-13 pm-2. A singlecell wall
has about 1500 perforations.They probably house plasmodesmata.
These results indicate that Sphagnum has an effectivemechanismfor
retainingand relocating solutes within it. This property,coupled with
the ability to grow in a very low supply of solutes, and to make the
environmentacid by cation exchange, may be seen as causes of the
widespread success of Sphagnum.
INTRODUCTION
Peatlands cover about 3 % of the Earth's land surface (Matthews & Fung I987).
The bog moss, Sphagnum,is an importantcomponentof a large part of this peatInstitutionen,Uppsala University,Box 559, S-751 22,
t Permanentaddress: Vaixtbiologiska
Uppsala, Sweden.
[ 63 ]
64
H. Rydin and R. S. Clymo
formingvegetation: it is not onlythe most importantbryophyte(in termsofmass)
but in the same categoryas the most abundant vascular plants. Unlike themit has
no anatomically specialized internalconductingsystem (Hebant I977) though it
does have an effectiveexternal water-conductingsystem.
An individual Sphagnum plant has a single apical cell in the centreof a domed
apex about 0.5-2 mm across. The apex develops primordia destined to become
stem leaves or branches. The branches in turn produce leaves. The crowd of
developing branches and leaves formsa dense mass - the capitulum - around the
apex. Internodes on the main stem then elongate thus separating the branches.
The branches are in fasciclesand, in most species, are of two sorts: spreadingand
pendent. In a carpet of Sphagnum the spreading branches of neighbouringplants
allow lateral transportof water (Clymo & Hayward I982). The pendent branches
forma capillary wick around the stem and provide an effectivevertical transport
path to the capitulum, the movement of water being driven by evaporation
(Hayward & Clymo I982). The much-vaunted hyaline cells in the leaves are not
directlyconcernedwithtransportas theyare, in effect,caverns that lead nowhere.
Differencesamong species in the abundance and size of pendent branches are
related to, and probably are the cause of, their ecological distribution(Hayward
& Clymo I982; Rydin I985).
External transportof water about Sphagnum is thus known to be effective,and
internaltransportofwater is comparativelypoor (Cavers I 9 II; Clymo & Hayward
Some mosses - Polytrichumfor example -do have specialized cells in the
I982).
these have a functionin transportingsolutes, but Sphagnum lacks such
and
stem,
It has thereforebeen generallyassumed that solutes are transported
differentiation.
about Sphagnum in the external stream of water. Yet thereare observations that
suggest that this may not be entirelytrue.
1. The concentrationon a dry mass basis of elements such as N, P, K, Mg and
S in the capitulumis greaterthan it is lowerdown the plants (Malmer I 962; Clymo
1978; Damman I978; Pakarinen I978; Malmer & Nihlgard I980; Malmer &
Wallen I986) and the upper parts of the plant retain almost all of the N, P and
K that fall on them in precipitation(Malmer I988). Most species ofSphagnum are
adapted to oligotrophicconditions- even quite low concentrationsof nitrate or
phosphate in water will kill them (Clymo I987) - so scavenging fromrain or dust
by the actively growingtissue might account forthese high concentrations.
2. In 1963 there was a peak in the influxof 137CS produced during testing of
nuclear weapons immediately before the U.S.A.-U.S.S.R. moratoriumon such
tests. Much of this 137Cswas mobile (a resultconfirmedby measurementsafterthe
accident at Chernobylin 1987) yet in 1973, ten years later, it was possible to find
a small peak in activity about 10 cm below the top of Sphagnum plants and a
much larger one in the capitula. About half the 137Cs that fell in 1963 was still
presentin capitula in 1973 (Clymo 1978). Again, scavenging may be invoked, but
in this case would have to be from upward transport. This seems implausible
because in the climate in which these plants grew precipitation much exceeded
evaporation for most of the year.
3. When brown and apparently dead Sphagnum from 30-40 cm below the
surfaceis exposed to air and lightthen innovations grow frompatches of cells on
TransportaboutSphagnum
65
the stem (Clymo & Duckett I986). Close to the surface,where the stem is still in
contact with the capitulum, innovations are rare except when the capitulum is
damaged. These observations suggest apical dominance controlledby hormones.
It is scarcely believable that the concentrationof hormonein an external stream
of water could be controlled,and thereforesome formof internaltransportmust
be invoked.
4. One interpretationof fieldexperimentsin which the top parts of Sphagnum
subsecundumtwere labelled with 14C(Skre etal. I983) is that therewas downward
transportfromthe green, apical part of the plant to the brown part below.
In this article we describe experimentsto seek direct evidence of the path of
transportof solutes about Sphagnum. We imagine threepossible routes: internal,
external in solution, and external in the gas phase. (This last route might be
significantforcarbon dioxide comingfromrespirationor fromdecay ofdead plants
of 32p (14 days)
belowthesurface.)We chosetwotracers:14C and 32p. The half-life
is sufficiently
shortthat the isotopes can be separated by makingrecordsimmedi-
ately(14C and 32p) and again afterseveralmonths(14C alone); and 14C mayreveal
gaseous transport.
We made three experiments.The firstwas to followthe physical and chemical
redistributionof 14C. It lasted four weeks and is referredto here as the C4
experiment.The second experimentwas to followthe redistributionof 14Cover a
longertime (22 weeks). We call it the C22 experiment.The thirdexperimentwas
to compare the movementof 14Cand 32p in differentflowregimesand to discover
the effectsof killing the stem. It lasted four weeks. We referto it as the CP4
experiment.
The order of the experimentswas determinedby practical considerations.We
present them in the order CP4, C4, C22.
METHODS
In all threeexperimentsSphagnum plants were labelled with 14Cor 32p then put
into a carpet ('matrix') of unlabelled plants in place of a plant removed fromthe
matrix. These carpets were in cylindricalpots or beakers of 10 cm diameter. The
cylindrical mass of plants had been collected in the field with a minimum of
disturbance using a corerwith a diameter of 10 cm. The experimentswere made
in a cool north-facingglasshouse on the roof of a building in London at times
between August 1987 and March 1988. Heating kept the temperatureabove 5 ?C
and during the winter natural daylight was supplemented by mercuryvapour
lamps givinga fluxat the plant surfaceof about 250 IEt m-2 s-5. The lightswere
on between 04hOOand llhOO, and again between 13hOOand 20hOO,thus leaving
a 'dark' period of 8 h.
Five species were used. Sphagnum fuscum, S. tenellumand S. balticumwere
collected in July 1987 fromthe ombrotrophicmireRyggmossen,Uppland, eastern
Sweden, at which place they are the commonest species. Sphagnum papillosum
t NomenclaturefollowsHill in Smith (I978).
t 1 einstein(E) = 1 mol photons; 1 ,uE = 6 x 1017 photons.
Vol. 237. B
66
H. Rydin and R. S. Clymo
were collectedin England fromCranesmoor(National Grid
and S. recurvum
Mire(TF 676288)
SU 185029),MoorHouse (NY 760325)and Dersingham
reference
at varioustimesbetweenSeptember1987 and February1988.
The 14Cand 32Pfour week experiment(CP4)
ofthetracersinSphagnum
was designedto showthemovement
Thisexperiment
plantsaroundwhichthewaterflowwas upward,downwardor still,and to show
ofkillinga smallpart ofthe stemon tracermovement.
the effects
Green shoots (7 cm long) of S. recurvumwere labelled with either 14Cor 32p in
the top 0-1 cm (capitulum),the middle3-4 cm or the basal 6-7 cm section.The
shootslabelledin the middlewereoftwo types:intact,and previouslysteamed.
consistedofplayinga jet ofsteamfroma Pasteurpipette
The steamingtreatment
above and belowtheas yetunlabelled
for30-40 s on sectionsof1 cmimmediately
3-4 cmsection.The sectionto be steamedwas grippedlightlybetweentworubber
bungshavingcentralholes.The steamwas passedintooneholeovertheplant,and
out oftheotherhole.The rubberservedto protecttheplanton eitherside ofthe
steamedsection.After1-2 days the steamedzones turnedwhiteand did not
The unsteamedpartsoftheplantsbothabove and
recoverduringtheexperiment.
belowremainedgreen.Steamedplantsgrewas muchas intactonesdid duringthe
experiment;the zone ofactivegrowthwas well above the steamedzone.
Tracerswereappliedto the appropriatesection:32pin NaH2PO4 at a rate of
4 gCit in 10 pl; 14Cin NaHCO3 at a rate of 1 giCiin 25 gil(capitulum) or 0.4 giCiin
10 gl (othertwosections).The untreatedpartswerecoveredwithaluminiumfoil
and the restilluminatedfor6 h. The treatedplantswerethenwashedtwicein
distilledwaterand put intoplace in a carpetofunlabelledplantsofdepth9 cmin
plants and three32P-treated
a beaker.Each beakercontainedthree14C-treated
lid covered
in a regulargrid.A gas-tighttransparent
plants,arrangedalternately
the beaker.
The beakersweregivenone ofthreeflowregimes(Clymo& Mackay I987).
1. Upwardflow.Air,driedoverCaCl2,was pumpedin througha holein thelid
and escapedthroughanotherhole,causingevaporationaveraging1.1 mmperday.
The beaker,whichhad a holein its base, stoodin a box withinwhichwaterwas
keptat 1 cm depth.Waterlost by evaporationwas thusreplacedfromthe box.
probablyoccupieslessthan0.5 % ofthecarpetcross
The pathofwatermovement
section,so the velocitywas probably10-20mmh-'.
2. Downwardflow.Distilledwaterwas sprayedon theplantseveryotherday
at a rateof1.8 mmperday,thesurplusescapingthrougha holein thebase ofthe
beaker.
3. No flow.No wateradded or removed.
In (2) and (3) thelidswereremovedfora fewminuteseveryday to allowsome
gas exchange.The waterlevelinall beakerswas keptat 8 cmbelowtheinitiallevel
of the capitula.
thuscontainedtwotracers(in thesamebeaker);four
Thisfactorialexperiment
modesofapplication(capitulum,middleintact,middlesteamed,basal); threeflow
t 1 curie (Ci) = 3.7 x 1010Bq.
67
Transport about Sphagnum
regimes; and two replicate beakers. The beakers were in two randomized blocks in
the glasshouse,and receivedsupplementarylight.The beakers werere-randomized
half-waythroughthe experiment,which lasted for30 days from9 December 1987
to 8 January 1988.
Two treated plants fromthe start of the experimentand one or two fromeach
beaker at the end of the experimentwere blotted dry then pressed flat between
absorbent paper and allowed to dry in air. They were transferredto X-ray filmfor
autoradiography.Afterthis they and two dried matrix plants fromthree beakers
were cut into 1 cm sections,weighed,thengroundin a mortarwith6.5 ml ofwater.
A subsample of 1.5 ml of this macerate was transferredto tubes containing3.5 ml
of Instagel. Light flashes were counted with a Packard 360 liquid scintillation
by 14Cwas avoided by countingin an energycounter.In 32p counting,interference
window centredon 32P and well above that of 14C. Quenching was negligible,and
was almost the same for all sarnples. Results were corrected for background
activity. In 14C counting,interferenceby 32p was avoided by making 14C counts
aftertwo months,when 32P activity had reduced to about 5 % of that when the
plants were killed. Correctionswere made for quenching and background.
The 14C four weekexperiment(C4)
This experimentwas designed to followthe movementof 14C (which may travel
by the internal, external and gaseous paths) in more detail, and to follow the
chemical transformationsduringan ecologically moderate length of time. Shoots
(4 cm long) of S. papillosum were labelled by submergingthem in an upright
position in 330 ml of simulated rainwater to which 1 mCi of 14C as NaHCO3 had
-beenadded. The plants were leftin the sealed container in daylight for 8 h. The
shoots were washed three times in distilled water then transferredinto a matrix
ofunlabelled S. papillosum at natural densityin beakers. Four labelled shootswere
put, spaced out, in each of 24 beakers. Of these, 12 were shaded with black nylon
gauze (about 35 % transmission).The beakers wereput into tunnelsoftransparent
nylon film,relativelyimpermeableto gases, in the glasshouse. Moistened air was
passed throughthe tunnels and C02 trapped in NaOH solution at the outlet. The
trap was changed at each plant-sampling.The water level in the beakers of plants
was kept at 2.5 cm below the top of the capitula.
Two shaded and two unshaded beakers were sampled immediately(0), and after
0.5, 1, 3, 9 and 27 days (between 22 September and 19 October 1987).
One labelled shoot and adjoining matrix plants fromeach beaker were blotted,
flattened,dried, and put onto X-ray film.The other three labelled shoots were
divided into capitulum (0-1.5 cm), and the lower 1.5-4 cm stem and branches.
Some branches were brownishin colour. The plants were put into 10 ml of 70%
ethanol at 4 0C for 3 days. After extraction the shoots were washed twice in
ethanol, dried and weighed. Two 5-10 mg subsamples were dried, ground in a
mortar, and a subsample added to Instagel before counting, as in the CP4 experiment. Subsamples of the NaOH trap were diluted and their radioactivity
counted. The results were correctedfor quenching and background.
The alcohol extracts were separated into cationic, anionic and neutral fractions
(corresponding,in the main, to amino acids, organic acids and sugars) by passing
3-2
68
H. Rydin and R. S. Clymo
them successively through Dowex 50 and Dowex 1 ion-exchange resins. The
radioactivityin each extract was estimated on a 25 gl subsample. Cold standards
were added to each fraction,then the constituentswere separated by two-way
paper chromatographyon 25 cm x 20 cm Whatman 3 MM paper. The cation
fractionwas separated by using phenol: water (100 g :33 ml) and butanol: acetic
acid: water (90:10: 29 by volume). Amino acids were located with ninhydrin.The
anion fractionwas separated using phenol: formicacid: water (100 g: 10 ml: 29 ml)
and the organic phase of tert-amylalcohol: formic acid: water (80:10:40 by
volume). Organic acids were located with a combination of NH4SCN and FeCl3
solutions in acetone (Firmin & Gray I974). The neutral fractionwas separated
(Calvin-& Bassham I957) by using phenol: water (100 g:39 ml) and n-butanol:
propionic acid: water (92:47 :61 by volume). Sugars were detected with saturated
AgNO3in acetonefollowedby 0.5 M NaOH in acetone(FirminI973).
Autographs
of chromatogramswere made on X-ray film.Radioactive spots were eluted and
their activity counted.
The 14C 22 weekexperiment(C22)
The C4 experimentshowed that a lot of 14C remained in the soluble phase fora
surprisinglylong time. We thereforetried in the C22 experiment to follow the
incorporationof14Cinto the insolublephase fora much longertimeand in a variety
of species.
Shoots ofS. fuscum,S. tenellum,S. balticum,S. recurvumand S. papillosum were
used. At the start of the experiment the shoots were 4 cm long, except for
S. tenellumforwhich the greenpart of the plant was less than 4 cm long. For this
species we used 3 cm plants. The central, shortest,branch in the capitulum was
marked by a dot of red spiritink, and the firstfullyexpanded branch by a dot of
black ink,to allow us to distinguishnewlyformedbranchesfromthose that already
existed at the start of the experimentbut which were carried up passively by the
elongation of stem internodes.Material above the red mark was whollynew; that
between red and black was partly new and partly old; that below the black mark
was almost all old.
The marked shoots were labelled with 14C in the same way that those of
to
S. papillosum had been in theC4 experiment.The labelled shoots weretransferred
a matrixofplants ofthe same species. The numberoflabelled shoots in each beaker
was determinedby theirsize and the fielddensity.It was: S. fuseum8; S. tenellum
8; S. balticum6; S. recurvum4; S. papillosum 4. For each species there were two
unshaded beakers and two shaded ones (as in experimentC4). The beakers were
put inside nylon filmtubes and air was passed slowly throughthe tubes. Carbon
dioxide was trapped in NaOH solution. For part of the experiment separate
collectionsweremade duringthe day and duringthe nightto seek diurnalpatterns.
The experimentwas made from22 October 1987 to 22 March 1988.
At harvest one labelled plant fromeach beaker was dissected into the belowblack, black-red and above-red (old, mixed and new) sections. These were dried,
weighed, and their 14C activity measured as in the C4 experiment. The same
measurements were made on two shoots of each species from the start of the
experiment(with no above-red section of course) and on two matrix plants from
one beaker foreach species.
Transport about Sphagnum
69
Scanning electronmicroscopy
Pieces of stem of S. recurvumwere soaked for 30 min successively in 70 %
ethanol, chloroform,methanol, and acetone to remove the contents of the cells.
The stems were then put into absolute ethanol beforecritical-pointdrying.The
dried stem was sectioned (or split) with a razor blade. The sections were then
sputter coated with Au and Pd and examined in a JSM 35 scanning electron
microscope operated at 20 kV.
RESULTS
The 14Cand
32P
four weekexperiment(CP4)
among the flowregimes,
An analysis ofvariance showed no significantdifference
indicating that mass transportin the external solution was unimportantin this
experiment.
positions and of steaming sections of
The effectsof puttingthe label in different
stem are shownas autoradiographs (figure1). Quantitative results,combiningflow
regimes,are shownin figure2. There was negligibleactivityin the water surrounding the plants. Where tracerhad been applied to the capitulum (0-1 cm) therewas
no indication of downward (basipetal) movement duringthe experiment,though
5-10 % had spread down during the initial labelling, perhaps by capillary movementamong the pendent branches. Where tracerwas applied in the middle section
(3-4 cm) about 45 % of 14Cand 30% of32P had moved to the capitulum by the end
of the experiment.There was no evidence of downward movement.Where tracer
was applied to the basal section (6-7 cm) there was upward redistributiontoo:
about 25 % of 14Chad moved to the capitulum, whereas about 30% of 32p was
fairlyuniformlyspread up the whole length of the plant.
The most importantresultmay be seen with the plants that were labelled in the
middle after the sections above and below (2-3, 4-5 cm) had been steamed. In
these cases there was no evidence of movement of either 14C or 32P during the
experiment,though some tracer had moved (during the initial labelling) outside
the segment to which it had been applied.
The radioautographs show the distributionin some detail. Where 14Cor 32P has
moved acropetally it seems to be in high concentrationin the stem and in the tips
of capitulum branches.
High concentration does not necessarily indicate the path of movement of
course: just as plausibly it indicates a sink of accumulation. But the absence of
any effectof flowregimecoupled with the results of steaming sections of stem do
indicate that most of the transportin this experimentwas inside the living stem.
The 14C four weekexperiment(C4)
Analyses of variance of the activityin soluble and insoluble fractionsshowed no
significanteffectof shading so the resultsforshaded beakers were combined with
those for unshaded ones in furtheranalyses. The pattern of changes when the
results were expressed on a dry mass basis was very similar to those on a plant
basis, so only the latter are shown.
The general pattern of change is shown in figure3. About 30 % of the 14Cin the
70
H. Rydin and R. S. Clymo
plants at the start of the fourweek experimentwas released duringit: about 8 %
(of the original) was found in neighbouringplants (almost all in their capitula),
and about 18 % in the NaOH trap. About 4% was unaccounted for.
The net loss fromlabelled capitula (21 %) was less than that fromstem and
branches below (48 %). In the capitula there was a threefoldincrease in activity
in the alcohol-insolublefraction,at the expense of the soluble fractions,particularlythe neutralone. In stem and branches,however,therewas littlechange in the
insoluble fraction.Activityin the soluble fractionsdecreased, but by less than it
did in the capitula. We suppose this decrease resulted fromrespiratorylosses and
frominternal transporttowards the apex, as we found in the CP4 experiment.
Changes in the capitula representthe net effectsof importthroughthe stem and
export to neighboursor out of the carpet of plants altogether.
The mostheavily labelled amino acids (table 1) wereasparagine (whichincreased
in relative importance over the 27 days of the experiment), and glutamic acid
which decreased. Together they constituted 65-80 % of the labelling. Other
labelled amino acids were aspartic acid, glutamine, arginine,valine and leucine.
acid (PCA), a breakAbout 20 % of the activity was in pyrrolidone-5-carboxylic
down product of glutamic acid or glutamine.
Only some of the labelled compounds in the anionic and neutral fractionswere
satisfactorilyidentified.Malic acid increased from 15 to 70 % of the anionic
fractionduring the experiment. More than 50 % of the neutral fractionwas in
glucose and fructose.
All these changes must be seen against a background of general decline in the
soluble fractions:the proportionof individual compounds may have increased but
their absolute activity decreased.
The 14C 22 weekexperiment(C22)
During the fivemonthsfrommid-Octoberto mid-MarchS. papillosum extended
least (6 mm unshaded, 17 mm shaded) and S. recurvummost (55 and 83 mm).
Details may be seen in figure4. Sphagnum recurvumwas noteable forshowingnot
only a large increase in lengthin the 'mixed' section (betweenred and black dots)
but also in the 'old' section (below the black dot). For this species internode
elongation continues more than 1 cm below the top of the capitulum.
The dry mass of the new section is a conservativemeasure of dry mass growth:
it makes no allowance for increase in the mixed section. Dry mass growth was
poorlycorrelatedwithgrowthin length,rangingfrom1.9 mg (S. fuscum)to 7.8 mg
(S. papillosum). These differencesoccur because the plants differin diameter.
DESCRIPTION
OF PLATE
1
FIGURE 1. The CP4 experiment.Plants labelledwith14Cin capitulum('top'), basal 1 cm,middle
1 cm,and middle 1 cm aftersteamingthe sectionsimmediatelyabove and below,together
with autoradiographs.The leftmostof each pair is immediatelyafter labelling; the
rightmostis afterfourweeks growthin beakers with downwardwater flow.The arrows
show wherethe radioactivesolutionwas applied. Verticalbars indicatesteamed sections.
The activityin each 1 cm section is expressedas the percentageof total activityin the
shoot.
Rydin & Clymo,plate 1
Proc. R. Soc. Lond. B, volume237
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Fordescription
see opposite.
Transport about Sphagnum
71
Analyses of variance showed that shading had no significanteffecton the
concentrationor proportionof radioactivity,either as a main effector in interactions, so the results forunshaded and shaded plants were combined.
The proportionofradioactivitystillpresentat the end ofthe experimentranged
from28 to 44% forfour species (figure4). This suggests a half-lifein the plants
of 12-19 weeks. The fifthspecies, Sphagnum recurvum,appears to have retained
almost all its label, a result we cannot explain. In all species the concentrationof
14C in the wholly new section at the end of the experiment is similar to that
remainingby then in the mixed and old sections (figure5). In many cases it was
greater. Only in S. recurvumwas it rather less. There had been compensating
decreases in concentrationin the old and mixed sections during the experiment,
except in S. recurvum.
The proportionof activity in the differentsections showed a similar pattern in
all species, with old, mixed and new sections having about 40, 35 and 25 % at the
end of the experiment(figure5) compared with about 65 and 35 % in the old and
mixed sections at the start. Again S. recurvumis rather different.
These differencesare reflectedin the analysis of variance at the end of the
experiment(table 2). 'Species' has a big effecton concentration,and 'section' on
proportion. In both the differentbehaviour of S. recurvumcauses a significant
interaction.
Some activity was found in neighbouringmatrix plants: about 1-2 % in this
experiment.The ratio of rates of CO2 trapping in NaOH during the day to that
duringthe nightwas 1.0: 2.8, indicatingthat the rate of CO2 effluxduringthe day
is only 36 % of that at night.
Structureof stemsof Sphagnum
The structure of Sphagnum stems differsamong species (Nyholm I969). In
S. recurvum,as figure 6 shows, the whole stem is parenchymatous. It snaps
suddenlyifbent. The parenchymais 20-50 cells across, each cell being of diameter
about 10 and 20 ,umin the outer and innerparts ofthe stem,respectively.The cells
are about 100-200 gm long.
The longitudinalwalls ofthese parenchymacells are almost imperforate,but the
end walls are densely perforate.The holes are about 75-100 nm across (figure6)
and at a densityof 7-13 pm-2. A single end wall has about 1500 perforations.We
assume that in life the perforationswere filledby plasmodesmata. Similar perforationsoccur in primarypit fieldson the walls of parenchyma in the stem apex
of S. recurvum(Baker I988). This density of perforationsis similar to that in the
DESCRIPTION
OF PLATE
2
at 3-5 cmbelowtheapex. (a) Transverse
FIGURE 6. StructureofthestemofSphagnumrecurvum
(hand) sectionoflive stem,mountedin water,lightmicroscope,100 gm (0.1 mm)scale bar.
Note the absence of a conductingstrand. (b) Longitudinallyfracturedstem preparedas
describedin the text,s.e.m., 100 gm scale bar. Elongate cellswithhorizontalend walls. (c)
Transverseend wall preparedas describedin the text,s.e.m., 10 gm scale bar. Most ofthe
cytoplasmhas been removed.Numerousperforationsare just visible. (d) Part of a transverse end wall showingperforations,
s.e.m. 1 gm scale bar.
H. Rydin and R. S. Clymo
72
top labelled
100
100
50
50
0
mid labelled
100
100
t 4 weeks
50
0
0
4 00
50
0
0
0
o
~
~'~
50
0
~
mid labelled and
0 steamed
100
I t---USl-
,\,
N
o
,'"50
1
0
0
andsea/me
mdislanebelled
base labelled
100
100
14C
50
50
0
32P
2
4
0
2
6
distance below apex/cm
4
6
FIGURE~2. The CP4 experiment.Activityof14C(top) and 32P (bottom)in 1 cm sectionsofshoots
as the percentageof total activityin the shoot. Solid lines show resultsimmediatelyafter
labelling(.T,n = 2); brokenlines are resultsafterfourweeks (.T,s.e.m., n = 6 fortop and
(see text)
base labelled,n = 5 formiddlelabelled). Resultsforthe threewaterflowreigimes
are lumped.Duringthe fourweeksof the experimentthe apical internodeshad elongated.
Distances were measuredfromthe shoot bases, and the nominal0-1 cm sectionincludes
that materialnow above the originalzero datum.
73
TransportaboutSphagnum
wholeshoot
insoluble
capitulum
t
6
4 _ f
w
2
~~~~~~stem
10
0
20
total
10
neighbours
and
gas
obranches
unaccounted
for
30
capitulum
5
~
neutral
wO 8 |
o
---)
20
tO
time/days
0
4
S
stemand
branches
30
2.
x
?
10
0
20
30
0
4-
total
10
0
10
20
30
4
-
<
4
inoul
~~~~~insolulble
cationic
0.6
_
cationic
0
0.4
20
10
time/days
anionic
30
neutral
0.2
0
20
10
time/days
30
FIGURE3. The C4 experiment.Time-courseofconcentrationof14Cin variouschemicalfractions
(insolublein 70% ethanol,neutral,anionic and cationic) and physicalpositions(stem+
branches,capitulum,neighbours,gas, and unaccountedfor).The graphson the leftshow
individualtraces; those on the rightare cumulative.
74
H. Rydin and R. S. Clymo
.+
t
io
(a)
tunshaded
120
120
f80
haded~
e
(b)
.
hddjnew
original shaded
unshaded
0
/
i
lmixed
g
40
old
S. papillosum
S. tenellum
S. fuscum
S. balticum
S. recurvum
S
100
k
4-)
(c)
80
60 20~
40
FIGURE4. The C22 experimentwith fivespecies. At the start the youngestbranch and the
youngestfullyexpanded branchweremarked.At the end ofthe experimentafter22 weeks
everything
belowthe lowermarkis 'old' mass; betweenthe marksis 'mixed' old and flew;
above the top markis 'new'. (a) Mean drymass (n = 2) in the new sectionin unshadedanld
shaded conditions.(b) Mean originallength,and lengthafter22 weeks in unshaded and
shaded conditions(n = 2); S. tenellumplants were 1 cm shorterthanithoseof'otherspecies
at the startand appear in the diagramon a pedestal. The two brokenlineslinkilng
sets of
columnsdraw attentionto the positioniof the marksseparatingoriginial,
mixed,anldnew
sections. (c) Mean proportionof 14C activity present in the plants at the start of the
experimentand still presentin the plants after22 weeks (n = 4).
TABLE 1. 14C ACTIVITY
OF TOTAL
IN AMINO ACIDS
ACTIVITY
IN THE
SPOTS
AFTER
0.5, 9 AND 27 DAYS AS A PERCENTAGE
DETECTED
0.5 days
glutamicacid
asparagine
PCA
aspartic acid
glutamine+ arginine
37
28
23
8
4
ON THE
AUTORADIOGRAM
activity(%)
9 days
35
48
17
n.d.
n.d.
acid.
PCA, pyrrolidone-5-carboxylic
n.d., not detectedon the autoradiogram.
27 days
17
66
17
n.d.
n.d.
TransportaboutSphagnum
S. fuscum
0.4
0.2
100
L50
[t
S. tenellum
0.4
100
'c0
t
0.6
0.6
..
0.4 .
|
>
t=O
100
t
5 months
50
S. papillosum
o
0
.,.0
.C 0.8
o
E
0!
?
S. balticum
?0.2
-4-
L
50
0.2
g
75
0
0.6
0.4
100lO
5
0.2
0
S. recurvum
0.4
100
r
50
0.2
old
mixed
new
old mixed
new
5. The C22 experiment.Distributionof 14Cin old, mixed and new sections of five
Sphagnum species immediatelyafter labelling and after 22 weeks (mean and range).
Hatched bars: at start (n = 2); open bars: after22 weeks (n = 4). The new section was
formedduringthe experiment.The leftdiagramsshow concentrationof 14Cin the plant
parts and the rightdiagramsshowproportionaldistributionof 14Cas the percentageofthe
total activityin the shoot.
FIGURE
TABLE
2. SUMMARY
TION
AND
OF THE ANALYSES
AND PROPORTIONAL
OLD
SECTIONS
source
section
species
sectionx species
error
OF VARIANCE
DISTRIBUTION
OF THE
FIVE
d.f.
2
4
8
45
SPECIES
OF RADIOACTIVE
OF 14C IN THE
SHOOT
OF SPHAGNUJM AFTER
concentrationof
radioactivity
F
1.26 n.s.
19.7***
2.17*
CONCENTRAIN NEW,
FIVE
MIXED
MONTHS
activityin section
total activity
F
28.0***
+
2.72*
d.f.,degreesof freedom;n.s., not significant.
* p <0.05; *** p <0.001.
+, each species totals 100%.
76
H. Rydin and R. S. Clymo
deuter cells of Dawsonia polytrichoides(Hebant I977) and in end walls of parenchyma cells of Polytrichumcommune(Eschrich & Steiner I968) whereas the
density in the oblique end walls of leptoid cells in P. communeis about twice as
great. The individual holes in S. recurvumare of similar dimensions to those in
P. communeleptoids and Dawsonia polytrichoidesdeuters.
DISCUSSION
Are metabolitestransportedin Sphagnum stems?
The usual view of transportin bryophytesis that wherethereis a differentiated
tissue in the stem, with specialized elongated cells resemblingthose in vascular
plant xylemor phloem,then one may expect to findevidence ofinternaltransport.
Polytrichumis a clear case. It has specialized cells - leptoids and hydroids- and
there is experimental evidence of transportof 14Cin the stems both above and
below ground (Eschrich & Steiner i967; Collins & Oechel I974). Trachtenberg&
Zamski (I978) suggested that transportmay occur in the symplast.
There has been a general presumption,however, that those mosses that lack
obvious specialization of the internal tissue of the stem, such as Sphagnum,
probably do not have a specialized system of transport inside the stem though
Hebant (I 977) pointed to indirectevidence of transportin Mnium and Dicranum,
both of which lack leptoid-likecells. Our observation of about 1500 perforations
in the end wall of otherwiseunremarkableparenchyma cells in the stem (figure6)
now provides a mechanical structurethat may plausibly be consideredthe seat of
transportprocesses.
Our CP4 experimentwith14Cand 32p tracersin S. recurvumshows clear evidence
that there is transportin the stem. The direction of mass flow in the capillary
system outside the stem had no detectable effecton the transportof either14Cor
32p, and this argues against passive transportin somethinganalogous to a transpiration stream. This conclusion is supported by the discovery that transport
was prevented when the stem was killed by steaming. We conclude that in this
experiment,at least, much the most importantmechanism of transportoperated
inside the stem.
The transportseems to be entirelyacropetal in this CP4 experimentwith plants
of S. recurvumthat were green throughtheir whole length. There is evidence of
acropetal transportin Marchantiapolymorpha(Rota & Maravolo I975; Gaal etal.
In Polytrichum,transportoccurs to undergroundaxes as well as to apices
i982).
(Collins & Oechel I974), and there is evidence of transportfromgametophyteto
sporophytein several cases (Proctor 1977, I982; Thomas etal. I979). There is one
report (Skre et al. I983) of basipetal transportin S. subsecundumlabelled in the
fieldwith 14Cin CO2. After2 h about half the activity was in the green section of
the plants and the rest in the underlyingbrown section. Results for the next 35
days were rather erratic but in general showed that 60-90 % of the label in the
green shoots disappeared whereas the amounts in the brown section decreased by
less or, in one case in autumn, increased. The authors concluded that there had
been basipetal transportbeforethe onset of winter.But it seems equally plausible
that there was a slower rate of loss fromthe brown section, consistentwith the
77
TransportaboutSphagnum
The extentofinitiallabellingin thebrown
resultsofourC4 and C22 experiments.
sectionremainspuzzling.
Relative rate of transferof 14C about Sphagnum
To tryto disentanglethe dynamicsofthe transportand chemicaltransformation
processes we now consider a simple model of the processes (figure7). It follows
conventionssuggested by Forrester(i 96I): full lines representflowsof substance
(14Cin this case) and brokenlines are flowsof information.We assume that all the
flowsof 14Care directlyproportionalto the size of the source, and are unaffected
by the size ofthe sink. Implicit is the assumption that ifthe drivingforceis related
then thereare negligiblechanges in the volume of the
to concentrationdifferences
compartmentsand that the concentrationin the net receivingcompartmenthas
a negligibleeffect.For the four weeks of this experimentthe firstassumption is
probably true to within 10% or so. The justificationfor the second assumption
differsfordifferentcompartments.In the case of gas the concentrationin the gas
phase remains very low as gas is removed; in the case of neighboursthe concentration of 14C is much less than it is in the treated plants; in the case of transfer
fromthe soluble to the insolublefractionin the capitulum the evidence shows that
the net movement is stronglyto the insoluble fraction; and the same argument
applies to the transferfromolderparts to the capitulum. None ofthisdemonstrates
that the sinks have no effect,but fora firsttrial the assumptions seemed to us to
|
gas (g)
l
(cs2ci
_s
FIGURE
4
7. Modelofflowi
V
)_
~~_
W
t-~~~~~~~~~
capitulum
soluble (es)
& branches,
~~stem
l
capitulum
insoluble
(6i)
y;
/
sbs2n)
sbs2gJ _---soube-(bs)--
insoluble(sbi)|
(sbs2sbi ----)
7. Model of 14Cflowin Sphagnum.Conventionsare thoseofForrester( I 96 I ). The boxes
FIGUPRE
fractions.These same fractionsweremeasuredat intervals
representamountsin different
in experimentC4. Solid lines show flowOf14C; brokenlines are flowof informationand
indicatecontrolof the valves. In all cases we assumed a simpleproportionalcontrol:the
ratesofflowweredirectlyproportionalto theamountin each box (see textforexplanation).
shownencircled.
coefficient,
Each valvealso has a rate-control
78
H. Rydin and R. S. Clymo
be acceptable. It is importantto realize that what we are followingis the transfer
of 14C, not total change in the molecular species in which it is incorporated.
We use the median values of the C4 experiment (figure 3), thus avoiding
problems created by the occasional extreme value.
The total 14C on a shoot basis, relative to the largest value (at 0s5 days) is shown
at the rightof figure8. Relative totals for0.5, 1, 3, 9 and 27 day samples ranged
between91 and 100 % withno obvious pattern.The '0' day sample had only 80 O/).
The proportionsof the differentcomponents in this sample were very similar to
those in the 0.5 day sample, however. As we are concerned with changes in
proportionswe decided (a) to omit the 'O' day sample and (b) to scale samples on
differentdays to the same total (100).
2
0
;
capitulumsoluble
(cs)
40
50
capitulum
insoluble
30
40
(ci)
2
20
30
3
30
20
20
0
10
30
13
27
1 3
9 27
gas (g)
10
?12
11
0
3
9
100
927
all compartments
1
02
3
9 27
0
o
30
1
rnhes
m
1 39
27
2
0
10
2
2
3927
neighbors n
insoluble(sbi)
10
1
time/days
stem& branches
soluble (sbs) ste
20
0
3 9 27
13
927
time/days
1~~213
927
time/days
time/days
the model shown in figure7. The first
FIGURE 8. Results of the CP4 experimentand of fitting
column (0.5 days) is used as the startingpoint forthe model,so thereis no fittedvalue
there.Hatched: fittedis less than observed.Dots: fittedexceeds observed.A '2' above a
column shows that observedand fittedare indistinguishableat this scale. The 'stem +
branches insoluble' fractionscarcely changes and was omitted fromthe minimization
times,
procedure.At the middlerightis the measuredtotal '4C on a shoot basis at different
relativeto 100 forthe sample at 0.5 days.
Figure 8 shows that the changes in the 'stem and branches,insoluble' fraction
were erraticand small. We thereforeomittedthe part of the model (figure7, lower
right) that concernsthis fraction.
This leaves six parameters- the rate coefficientsin figure6 - to be estimated.
Transport about Sphagnum
79
The initial values in the boxes are the 0.5 day results,thus leaving 20 independent
observationsto fitsix parameters,i.e. 14 independentvalues. It is obvious that we
should not expect to get highlyprecise estimates.
In operationwe chose parametervalues arbitrarilythenran the model offigure7
with 0.1 day incrementsto produce model values for each of the fractionsfor
whichtherewere measurements.The fitbetweenmeasured and modelled was poor,
of course. We then used a simplex technique (Nelder & Mead 1965) to adjust the
six parametervalues in such a way as to minimizethe sum ofsquares ofdeviations
between the measured and modelled values of the five fractions.Other criteria
gave similar results.
There is no way that one can be surewiththistechniquethat the global optimum
has been found but if one findsthe same point fromnumerous differentstarting
points and with differing
rates of contraction,and the fitto the data is good, then
it is reasonable to accept the best solution. We made 23 optimizations: each took
about 30-40 min on a microcomputer.Of these, 15 gave verysimilarvalues forthe
optimization criterion.The other eight were noticeably poorer. The 15 were not
identical: the greatest was 0.3 % larger than the smallest. To three significant
digits they all gave the same value for four of the six parameters (table 3). The
other two parameter values were four or five orders of magnitude smaller. The
values are shown in table 3, and the fittedvalues in figure8. Repeated location of
a similar set of values is satisfactory,though the precision with which the parameters are estimated is not great, and in the two cases of small values is very
poor.
TABLE
3.
ESTIMATES
OF VALUES OF THE RATE COEFFICIENTS
MODEL IN FIGURE 7
parameter
value
(% d-1)
pEa
cs2g
sbs2g
sbs2cs
0.060
2e-7 to 8e-8
0.063
0.11
+
0.14
cs2ci
cs2n
sbs2n
0.111
0.024
6e-6 to 2e-8
0.08
0.22
+
symbol
capitulumsoluble to gas
stem+ branchsoluble to gas
stem+branch soluble to
capitulumsoluble
capitulumsoluble to insoluble
capitulumsoluble to neighbours
stem+branch soluble to
neighbours
OF THE
standarderror/mean.
+, low precision.
a PE,
This model and optimizationlead to several tentative conclusions,perhaps best
treated as hypotheses worth furthertesting. They concern the rate coefficients,
which may be imagined as being the inherentconductances of the pathways. The
actual rates will depend on the drivingforcestoo.
(a) The rate coefficient
for,and the actual rate oftransferof,14Cfromthe soluble
fractionin stem and branches to either the gas phase above the Sphagnum or to
neighboursis verysmall, and negligiblecompared withtransportto the capitulum.
80
H. Rydin and R. S. Clymo
The rate coefficient
fortransportto the capitulum, 0.063 per day, is equivalent to
a half-timeof about 11 days.
(b) From the point of view of the capitulum, the rate coefficient
foreffluxof 14C
fromthe soluble fractionto the gas phase - respiration- is nearlythe same as that
of influxfromthe stem and branches below. The coefficientfor transferto the
insoluble phase is about twice as great, and of transferto neighboursis about half
as great,as that ofrespiration.In a completecarpet one mightexpect that transfer
of carbon-containingcompounds from neighbours would, on average, balance
losses to them.
Transport to the capitulum frombelow may be throughthe stem, around the
stem, or in the gas phase. It is possible to make a crude estimate of the proportion
of 14Ctransferredin the gas phase duringthe C22 experiment.The relative rate at
which 14C02 collected in the NaOH trap during the day and night was 1:2.8. If
we ignore diurnal changes in respirationrate then this implies that during the
16 h day an amount of 14C02 equal to 75?% of the amount actually trapped in
NaOH failed to reach the trap because it was reabsorbed by the plants: a total of
1.67 x 106 disintegrationsper minute (d.p.m.) per shoot.
The parameter values in the model indicate that transferfromthe stem plus
branch fractionwas almost entirelyto the capitulum, and this was about 26 % of
the total 14C(figure8). This gives 2.44 x 106 d.p.m. per shoot. An extremeview is,
then, that 1.67/2.44 (68%) of the transferis in the gas phase, and 32 % in the
stem.
A more plausible assumption is that 14C02 was evolved by the capitulum and
that some of this could be reabsorbed too. The capitulum contained about as
much 14Cin the soluble phase, on average, as was in the stem plus branch fraction
(figure8). This suggests 1.67/(2 x 2.44), or 34 %, oftransferis in the gas phase and
66 % in the stem.
In the CP4 experimentabout 45 % of the 14Cmoved to the capitulum, but only
30 % ofthe 32p. This resultis consistentwith the existence of an extra path for14C,
carryingabout one-third of the total 14Cthat moved.
The very small amounts of 14Ctransferredto the capitula of steamed plants in
the CP4 experimentand to neighbouringmatrix plants in all three experiments
suggest,however,that these may be over-estimatesof the importanceof the gasphase route.
In summary, Sphagnum papillosum has a mechanism that transferssoluble
carbon compounds fromthe older parts to the capitulum at a much greaterrate
than they are lost by respirationor transferto neighbours.The inherentconductance of this pathway - mostly inside the stem - is about the same as that of
respirationby the capitulum,and about halfthat at which soluble compounds are
transferredto an insoluble form.
These processes of predominatelyacropetal transportcontinue over long times
and in other species of Sphagnum, as the results of the C22 experiment(figure5)
show. Afterfivemonthsabout 25 % of the initial 14Chad appeared in totally new
growthlargely,we suggest, as a result of transportin the stem.
Transport about Sphagnum
81
The compositionof thesolublefraction
morecarbonintoorganic
Amongthesolublefractions,
Sphagnumincorporates
acids than into aminoacids, in contrastwithPlagiochilaasplenioides(Suleiman
betweenSphagnumand other
I98I). However,thisneednotindicatea difference
accordingto Maass & Craigie(I964) S. papillosumcontainsa lower
bryophytes:
concentrationof amino acids than otherspecies of Sphagnumdo (0.08% in
S. papillosumcomparedwithan averageof0.4 % in theelevenotherspeciesthey
60-70% ofthesolubleactivitywas foundin the
investigated).
In ourexperiment,
neutralfraction.
Thisis similarto thatinPlagiochila(SuleimanI98I). In an earlier
inS. papillosum
experiment
(ClymoI967) 41% of 14C was in the insoluble fraction
oneday afterlabelling,a valuethatwas reachedafterthreedaysinourexperiment
with the same species. With these comparisonsin mind,it seems likelythat
studies may
differences
in distributionamong fractionsobservedin different
genusor species
conditionsthanon thebryophyte
dependmoreon experimental
studied.The neutralfractionseemsalwaysto dominateamongthe solublefrac(Maass & CraigieI964; ClymoI967; SuleimanI98I).
tionsin bryophytes
Glucoseand fructoseare knownto be the mostimportantsugarsin Sphagnum
(TheanderI954; Maass & CraigieI964), and malicacid is a majorcomponentin
theanionicfraction(50-70% oftheorganicacidsfordifferent
speciesofSphagnum
(Maass & CraigieI964)). Our resultsshowthat 14Centersthesesame compounds
in large amounts. A similar pattern appears in the liverwortPlagiochila
are already
asplenioides(SuleimanI98I). All the aminoacids that we identified
knowninSphagnum.In additionto asparagineand glutamicacid (whichwe found
in greatestquantities),asparticacid, glutamine,serine,arginineand threonine
have been reportedas quantitativelyimportantin Sphagnum(Maass & Craigie
I964; Thones & Rudolph I983). The quotientbetweenthe amountsof 14Cin
quiteclose
asparagineand glutamicacid was 3.9 after27 days in ourexperiment,
inS. magellanicum
grownin culture(Thones
to a quotientof3.4 forconcentrations
& Rudolph I983).
The proportional
of14Camongfractions
appearedto be stabilizing
distribution
at theendoftheC4 experiment,
chemicalchangesafter27
indicatingthatfurther
days may be small. The upwardtransportof 14Ccontinuesinto newlyformed
in growthmorbiomass,however,as our C22 experimentshowed.Differences
in newbiomass
phologymayaccountforthesmallerfractionoftheradioactivity
formsless dense
in S. recurvum
than in the otherspecies.Sphagnumrecurvum
down,so
carpetsthantheotherspeciesand thisenableslightto penetratefurther
that a greaterproportionof the basal parts may be photosynthetically
active.
to keep
Because oftheremarkablegrowthin lengthofthisspeciesit was difficult
the shootstogetherand the lightpenetration
was even greaterthanusual. As in
the C4 experiment,
14Caccumulatedin the top section.
Ecologicalimplications
In its abundance,as wellas in anatomyand morphology,
Sphagnumis distinct
It can makethewateraroundit unusuallyacid (Clymo
fromall otherbryophytes.
I963; BrehmI97I ; ClymoI984) bycationexchangeofionssuchas Na', K+, Ca2+,
82
H. Rydin and R. S. Clymo
Mg21 in rainforH+ on theplants;it can tolerate(orevenrequires)unusuallylow
suppliesof inorganicnitrogenand phosphoruscompounds(Press et al. I986;
Rudolph& VoigtI 986; ClymoI 987); and ithas a remarkable
capacityforexternal
transportofwater(Hayward& ClymoI982).
The conditionsrequiredby,or consequentupon,thesethreefeaturesresultin
the accumulationof peat that is waterlogged,
acid and poor in solutes.This,in
turn,restrictsthe species of vascular plants to those that can toleratethese
conditions.
Manyoftheseshrubsconservenitrogen,
phosphorusand potassium(as wellas
organicsolutes)withinthem,shuttlingsolutesfromthe aerial parts to subterraneanroots,rhizomesor shootbases as winterapproachesand back to aerial
partsinspring
(see,forexample,
Seeb0I 968,I 970, I 973, I 977; Chapinetal. I 975;
Chapin& Bloom I976; Malmer& NihlgardI980).
It seemsclear that in theseombrotrophic
conditionsnutrientlimitationand
conservationare an importantfeatureof plant life.The workreportedin this
ar-ticle
allowsus to add the capacityto relocatesolutesinternallyas one of the
featuresof Sphagnumthat contributeto its success. The detailed mechanism
deservesfurther
investigation.
We thankProfessor
J. G. Duckettformakingthescanningelectronmicroscope
preparations;D. 0. Gray for advice about fractionationof solutbes;Mrs P.
Ratnesar,E. T. Haig and Folke Hellstromforpracticalhelpofvariouskindsand
the SwedishNaturalScienceResearchCouncilfora grantto H. R.
REFERENCES
Baker, R. G. E. I988 The morphologyand distributionof pits in the cell walls of Sphagnum.
J. Hattoribot.Lab. 64, 359-365.
Brehm,K. I97I Ein Sphagnum-Bultals Beispieleinernatiirlichenlonenlaustauchersaule.
Beitr.
Biol. Pfl. 47, 287-312.
Calvin, M. & Bassham, J. A. I957 The path of carbonin photosynthesis.
New York: Prentice
Hall.
Cavers,F. I 9 I I The inter-relationships
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Chapin,F.-S. & Bloom, A. I976 Phosphate absorption:adaptation of tundragraminoidsto a
low temperature,low phosphorusenvironment.Oikos26, 111-121.
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Clymo,R. S. I963 Ion exchangein Sphagnumand its relationto bog ecology.Ann. Bot. (N.S.)
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