Download The ecological significance of organochemical

Acta Bot.
Neerl.
46(2),
June
117-130
1997, p.
Review
The
ecological significance of organochemical
in
compounds
J.T.A.
Sphagnum
and
Verhoeven
W.M.
Liefveld
Department of Plant Ecology and Evolutionary Biology,
TB
3508
Utrecht University,
PO
Box
800.84,
Utrecht, The Netherlands
CONTENTS
117
Introduction
metabolites
Organic
118
produced by Sphagnum
Ecological significance
of the various organochemical
compounds
120
Final remarks
126
Summary
127
Acknowledgements
127
References
128
Key-words: allelopathy, bogs, decomposition, fens, peat acumulation,
plant metabolites,
phenolics, secondary
tannins.
Sphagnum,
INTRODUCTION
Peatlands
function
most
and
total
1991; Maltby &
storage capacity
primary
This low
peat
known
to
of
the
be almost
sition of peat
moss
specialized,
slow-growing
to
a
several
a
at
the
same
organochemical
suppression
of the
1997
genus
Royal
Armentano &
balance between
consumption
is related
to
the
of
Sphagnum
Hayward
if the material is
hollows and
bog
phanerogams
1995).
The
Their
sponge which holds
in
survive
success
1982),
by
have
structure
Sphagnum
Botanical
such
gives
them
phenolics
as
plant growth,
given
a
a
general
benefit
Society
to
over
as
well
as
and
litter
creates
high
a
cation
uronic
acids
of The Netherlands
plants
in
and
&
in
only
Van
Sphagnum
permanently
wet
exchange capacity
production
contributes
to
of
the
decomposition.
overview of the traits which
other
stands
respect has been
anatomy makes
and
a
this
a more
1993).
compact
conditions (During
genus in
and
very well
dense,
is
decompo-
transferred
time acidifies the environment and traps nutrients. The
compounds
animals
and
plant growth forms,
these
of the
morphology
water
plus
wet, acidic
& Butterfield 1978; Johnson & Damman
properties.
of vascular
Earlier reviews
&
1986;
through
far the
important peat-forming plants,
hostile environment for other
Their characteristic cell wall
which
©
create
most
(Clymo
even
lawns in
thick
Van Breemen
as
respiration
decomposition
by
are
of carbon stored
positive
a
carbon storage
bogs
amount
Menges
by
Consumption
bogs
notably slow,
(Coulson
form
They
carpets work
Sphagnum.
absent in
totally
hummocks.
attributed
and
long-term
a
total
covered,
Armentano &
1981;
consumption
litter is
Sphagnum species
1990;
area
total ecosystem
genus
favourable environment
Tooren
of
with
1993). Ombrotrophic
the chemical composition of the
to
mosses
terms
(Sjors
and
production
conditions and
soil.
in
Immirzi
The carbon storage function is caused
1990).
decomposition.
the
type of terrestrial ecosystem
only
important peatland type
Verhoeven
net
the
are
(Gorham
bogs
and
by
give representatives
which
they
create
and
118
J.
maintain their
Van Tooren
role of
plant
An
will
genus
be
of
types
and their
given,
Hayward
is
and other
1989),
VERHOEVEN
AND
W.
1982; Clymo
M.
i.e.
metabolites with
organochemical
chemicals
organic
supposed
or
LIEFVELD
&
1983b; During
the purpose of this review
metabolites,
secondary
overview of the
It
1995).
A.
&
(Clymo
Breemen
metabolism (Baas
Sphagnum.
of the
Van
1990;
greater detail the
in
environment
own
T,
address in
to
direct role
no
compounds
produced
by
produced by representatives
demonstrated ecological
significance
will be evaluated.
ORGANIC
METABOLITES
PRODUCED
BY
SPHAGNUM
Phenolics
A first
been
group of
major
existence
discovered
chemical
after
compounds
the
at
addition of Millon’s
substance
(1967)
isolated
They
different
eight
acid
he found
its
knowing
used
are
here
phenolics
to be
out
indicate the
indicated
are
a
According
cell
to
ring, respectively,
mixture of these
to
walls.
1973;
This
acid’ for this substance
acid
Sphagnum
isolated from
in
all
is
et
and
by
primarily
dation
and
Recent work
Rasmussen
all
in
associated
products
of
crystals
to
were
the
acid
and
the
and
the
polyphenolic
the
to
of
Conglomerates
found
turned
by Czapek
discard the
‘sphagnol’.
term
monophenolic
1971; Rudolph
the
among
Samland
in
various
(1985)
PTutschek
1972;
the
et
‘sphagnum
name
Several authors
cell
walls
on
(1995)
species
the
acid,
has
cell wall
acid,
as
well
buffer-soluble
been
the
to
a
phenolics
small
and
sphagnum
several
that
the
and,
form
to
Sphagnum
majority
therefore,
the peroxidative
of
not
degra-
hydroxybutenolide
p-coumaric
degree
that
assumed
in
phenolics
however,
contrast,
present
species,
on
1992; Van der Heijden
Rudolph
/;-hydroxyacclophenone,
as
only
In
compounds
was
depending
buffer-soluble
was
(Fig. 2).
i.e.
phenolic
suggested
has
it
of
revealed,
investigated
have
where
compartmentalization
al.
the
found that it
quantities
networks (Rasmussen &
sphagnum
p-hydroxybenzoic
cinnamic acid,
&
tested,
with
et
with
be
to
constituent
Rudolph
plant parts investigated.
acid
sphagnum
the
i.e.
,
1).
dominating
three-dimensional polymeric
1997).
As
‘sphagnol’.
groups bound
hydroxyl
more
&
Rudolph
of
magellanicum
1990). Rudolph (1972) proposed
representatives
mainly associated
al.
al.
spp.
seasons
et
shown
was
(Fig.
acid
species
or
walls
he named the
acid, vanillic (4-hydroxy-3-
Waterman & Mole (1994).
acid (Tutschek & Rudolph
the
Sphagnum
Sphagnum
is
one
of the
study
a
nature
monophenolic
components, they proposed
substance
also Wilschke
see
In
already
Engmann (1972), substance ‘D’ is responsible for the red coloration of the
(carboxymethyl)-cinnamic
al.
of
presence
polymeric phenols.)
as
had
(tra«,v-4-hydroxy-3-methoxy-cinnamic)
terms
The
phenolics.
structure.
chemical
p-hydroxybenzoic
proposed by
as
chemical
into the
unidentified substances ‘C’, ‘D’, ‘E’ and ‘F’. (The
aromatic
1913).
from the cell walls of S.
compounds
and ferulic
the
red coloration of the cell
a
exact
investigations
monophenolics p-hydroxybenzaldehyde,
methoxybenzoic)
are
and after isolation of the crystals
Reagent,
made detailed
Sphagnum
Sphagnum representatives
by Czapek (1899,
century
magellanicum,
without
‘sphagnol’,
Engmann
for
specific
of the
turn
of S.
composition
metabolites found in
secondary
of chemical
acid
primarily
and
bound
trans-
to
the
cell wall.
However,
habitats.
this
The
was
only
Sphagnum
©
1997
for
true
plants
Royal
the
grown
Botanical
Sphagnum
in
plants
bioreactors
Society
of The
collected in
showed
Netherlands,
their natural
dramatically
Acta
Bot.
Neerl.
46,
higher
117-130
ORGANOCHEMICAL
1.
Fig.
Chemical
structures
(b) sphagnorubin; (c)
2.
Fig.
cuspidatum.
to
cell
et
al.
0X5
of
some
of
in
the
field;
cultivated in bioreactors.
wall);
(1995),
black:
with
kind
permission
SPHAGNUM
molecules
119
discussed
in
this review,
(a)
sphagnum acid;
trans
acid.
Sphagnum.
Sm:
Sm;
Sphagnum magellanicum
Sphagnum magellanicum, cultivated
White: buffer-soluble
dioxane-extractable
fraction
from Elsevier
fraction;
(strongly
Science
bound
Ltd.,
in
collected
in
bioreactors;
grey; ethanol-extractable
to cell
The
the
field;
Sf:
,
wall). Reprinted
Sc:
Sphagnum
fraction
(bound
from Rasmussen
Boulevard, Langford Lane, Kidlington
1GB, UK,
buffer-soluble fractions for
caused
most
©
in
phenolics
collected
IN
important
5-keto-D-mannuronic
Concentration
Sphagnum fallax,
COMPOUNDS
the
cultivated
phenolics.
1997
Royal
most
of these
Sphagnum plants
The cultivations also
Botanical
Society
of The
compounds
to
produce
enabled
Netherlands,
(Fig. 2).
higher
measurements
Acta Bot.
Neerl.
46,
It is
not
known
what
buffer-soluble fractions
of
of concentrations of the
117-130
120
J.
in
phenolics
the
effluent
and
hydroxybutenolide
trations in the media
active
an
There
spp.,
to
VERHOEVEN
acid
130 and 130
mechanism
for
are
indications for
many
the
all details of their
not
existence of
chemical
exact
who assumed that
networks and that
for studies of the
Van der
by
derivatives,
acid
gallic
tannins.
hydrolysable
l3
C
using
Dawsonia (Wilson
indications for
et
of
among
acid,
concen-
&
(Rudolph
He detected
nuclear
magnetic
For
1989).
higher plants
the
structure
and
primarily
visualized
as
spp., Van der
network with
series of
complex
a
biosynthesis
structures
for
(NMR)
resonance
Sphagnum
in
lignin
phenolics trihydroxy-
both precursors of the
acid),
al.
Rasmussen
spectrometry (PYMS)
mass
trihydroxybenzene
of
contrast
networks
effect of
cellulose-masking
spp.
Sphagnum
the basic constituent of these
was
the monomeric
were
in
known. In
lignin. Polymeric
(trihydroxy-benzoic
occurrence
are
X-ray technique by
pyrolysis
Sphagnum
which
biopolymeric polyphenolic
a
an
no
The
tannins in
same
used
Heijden (1994)
organic chemistry
acids and
benzene and
strated
phenolics
polymeric phenolics
sphagnum acid
their function could mimic the
higher plants.
phenolic
these
contain
suggestions (Painter 1983), peat mosses
Rudolph (1992),
many
LIEFVELD
Trans-sphagnum
composition
associated with the cell walls have been detected with
&
M.
Sphagnum cuspidatum, respectively), and
for
postulated
was
1995).
W.
the substances with the highest
were
nM
al.
et
AND
1992).
although
earlier
A.
(Rasmussen
p-coumaric
(290,
excretion
Rasmussen
media
T.
the
bryophyte
Heijden (1994)
genus
found strong
with
comparable
a structure
of
demon-
was
associated with the cell walls. This may have been
with
the
used
X-ray technique
Rasmussen
by
&
Rudolph (1992).
A smaller
(Fig.
1).
polymeric polyphenol
This
anthocyanin
associated with
is
compound
conditions of temperature,
light
of Sphagnum magellanicum
in
and
red
a
and is
hormones,
&
(Clymo
autumn
Sphagnum
cell walls is
sphagnorubin
under certain
pigment which is formed
for the red coloration
responsible
Hayward
Gorham
1982;
Mues
1990;
1990).
Carbohydrates
A
second
major
10-30% of
the
compounds
walls
and
are
present
consist
mannuronic acid
&
(Clymo
in
the
well-known ion
The
(Fig.
the CH
carboxyl
as
1).
of
of
equal
Both
uronic
exchange capacity
polymerize
to
of
a
1983,
are
and
as
,
dissolved
sugars
The
1990).
Mg
2+
with
in
2+
called
covalently
the
is
cell
5-keto-Dcells
hyaline
carboxyl
a
and also acidifies the
which is
and
group
of the protons
exchange
Ca
or
substance
pectin-like
the holocellulose in the
acid
the
bog
basis
of
to
the
environment.
also
glycuronglycan,
linked
up
these
cellulosic and
chains in the cell wall.
(1994)
superficially
hydroxy
such
1991),
also
are
make
Most of
1987).
galacturonic
occur
acids
Sphagnum
Another feature characteristic of the
Heijden
of
which
acids,
(Clymo
associated with
compounds
cations
against
uronic
plants
side chain (Brown & Wells
OH
2
the
are
Sphagnum
quantities
These
sphagnan (Painter
amyloid-like
metabolites
living
long polymers
1982).
groups
uronic acids
known
as
mainly
Hayward
subsituting
of organic
group
dry weight
acids,
esterified
by
means
coated
and
of
PYMS.
by lipid
fatty acids,
with
phenolic
Sphagnum
cell walls
was
He
that
cell
found
substances such
probably
acids.
as
C
-C
20
associated
These
the
polymers
24
with
can
detected
wall
by
dicarboxylic acids,
the
be
epicuticular
seen
Van der
polysaccharides
as
C
-C
14
wax
26
layer
suberine-like
substances.
©
1997
Royal
Botanical
Society
of The
Netherlands,
Acta 801.
Neerl.
46,
117-130
ORGANOCHEMICAL
ECOLOGICAL
COMPOUNDS
of
production
large
conditions in which
low
to
such
phenolics
tannins
or
pathogens
in the
up
provide
or
This is referred to
later
slows
erably
down
decomposability
plant’s
these
general
ecosystem,
although
(Coley
al.
et
of
as
be
can
this
has
the
on
an
rely
to
known that
microbe attacks
be
attacked
‘almost
some
by
of
ecology
of the
have become
the
1993),
The demonstrated or
the
on
done
summary of the
the
bog layer
upper
where
deeper peat layers,
see
have
’
(Clymo
the
1994). Although
range of
large
1989).
than
of the
bog
Sphagnum,
As
incomplete.
large
amounts
J.
Hayward
&
been found
only rarely
Galerina,
genus
bogs
as
are
of second-
Wiegers,
et
personal
al.
1981;
1982),
( Sphagnum
and that
spp. may
communication).
Verhoeven
et
al.
1990;
and dead animal and human bodies buried in peat
(Painter
will
of the
Ingram
bogs
1991).
effects of metabolites
bog ecosystem
most
Litter
influencing
ecology
other
of
production
consid-
important compounds,
most
been
also
was
1987).
1989).
(Baas
in the
plants
on
be
the
on
reviewed
functions of the various
(possible)
and
al.
et
or
1986).
their function in the
by Sphagnum,
genus has
Sphagnum
eats
supposed
of the
functioning
Baas
of the
most
confidence for the
this
well conserved
extremely
tannins,
1988;
characteristic
role of
genus,
herbivory
al. 1983), which
is far from clear
Further, decomposition in bogs is very slow (Brinson
Johnson & Damman
and
(Nicolai
of
is in line with the ‘carbon/nutrient balance theory’. Also,
nothing
of
fungi
exact
by plants
studies
on
living peat mosses
on
litter
et
‘excess’
Rosenthal
1985; Bryant
including lignin
important plant
the
made,
partly
by Sphagnum
compounds
it is
al.
et
Under
terpenoids,
as
against
1971;
theory’ (Bryant
metabolites formed
secondary
chemical
defence
1985; Waring
generally extremely nutrient-poor systems,
ary
better
a
due
e.g.
1992).
an
such
compounds
pollinators (Levin
plant
formed
be indicated with
can
accumulate and
to
in nutrient-poor environments (Berendse
compounds
the
to
plant
attract
of the various representatives
autecology
research
to
has been indicated
secondary
tend
the form of
secondary metabolites,
statements
With respect
the
give
decomposition
fitness, particularly
different
in
under
occurs
circumstances,
Lambers & Poorter
1989;
carbohydrates
often
by plants
environmental
by
(Baas
water
or
mechanism
evidence
The accumulation of
VARIOUS
metabolites
secondary
is restricted
plant, mostly
which
a
THE
the ‘carbon/nutrientbalance
as
supported by
of
amounts
plant growth
non-structural
conditions,
OF
121
COMPOUNDS
of nutrients
availability
carbon builds
SPHAGNUM
SIGNIFICANCE
ORGANOCHEMICAL
The
IN
ecology of Sphagnum
below.
takes
place)
and
contains
in the acrotelm
compounds
biological activity
Table 1
(i.e.
and the catotelm
a
the
(the
1983).
Ecology of Sphagnum
The
phenolic
component,
associated
strength
the
with the
and
the
after
of
©
lipid
to
their
surface
1997
bulk
Royal
walls locks
the
related
of
lignin
up
strength (Van
of the cell
and death of
the
creating
The
network
Heijden
walls,
also
1994).
of The
strongly
Netherlands,
the
hydrolysable,
The
al.
with
1988).
Acta Bot. Neerl.
46,
117-130
network
a
greater
condensed tannins
of
cell
walls
cellulose,
The slow
microbial
dominant
rigidity created by
inhibit cell wall
reduces
a
cell walls
the
masking
as
polymeric
the structural
strongly
et
acid
The
gives
associated
plant parts (Horner
polysaccharides
Society
cellulose and
higher plants.
der
sphagnum
plant’s functioning.
without
polyphenolic
coating
Botanical
in
with
Sphagnum,
for the
polymeric
senescence
the
cell
by
significance
water-holding capacity,
another
contributes
produced
of great
functionally
form
as
acids
are
which
as
well
decomposition
decomposition
immobilization of
122
J.
T.
A.
VERHOEVEN
AND
W.
M.
LIEFVELD
by
plants
demonstraed
Function
Acidfcation
function
diseases herbivoryDON
decompsitonvascular decompsiton decompositn against decompositn celuose
celuose
of
of
against
Inhibtion Inhibtion MMaasking Resi tance Resitance DDeefence Def nce
herbivory capacity capacity
protein
acids
decompsiton humic decompsoit n
Mobilzaton Inhibtoin MaMasking against exchange Acidfcation exchange Acidfcation Tan ing Inhibtion Formation Resitance
of
Def nce Cation
Cation
Italics:
&
Acro-/atelm
bogs.
peat
Acrotelm
&
&
Acrotelm catoelm Acrotelm catoelm
Catoelm Acrotelm Acrotelm Acrotelm catoelm Catoetlm
Acrotelm
of
catoelm
wall
water
bound
in
wall
wall
in
in
wall
Soluble,
Cell
Cell
Soluble,
Cell
Cell
Cell
Cell
Polymeric Mon meric
Polymeric
Polymeric
bog
bog
and
Solube/c l
acrotelm
watwater
bound
bog
bog
bound
bound
Soluble
wall
wall
bound
Soluble
wall
wall
the
in
Sphagnum
in
found
indcations
compounds through
as umed
organchemialfunction
of
Mon-/plymeric
acid
molecule
of
Type
Table
acid
Polyphenol,
Phenolic
tannin
acid,
hydrolysable
Polyphenol, anthocyani Galcturonic
coating phenolics
P5-ketoDmanuric olysachride, pectin-like
surface with
Lipid
as ociated
print:
Functions normal compound
1.
Mon meric Polymeric Polymeric
acid
evidence; Chemical Sphagnum
©
Sphagnorubin
Tan in
1997
Royal
Botanical
Society
acids
Uronic
of The
s.l.
Sphagna n (glycuronglyca )
Netherlands,
acids
Fatty
Acta Bot.
Neerl.
46,
117130
ORGANOCHEMICAL
nutrients,
COMPOUNDS
there
have
microbial attacks
parts of the
living
been
few
is
these cell wall-associated
of the
autolysis
plant (Damman
studies
living Sphagnum
on
123
SPHAGNUM
that the nutrients released after
so
available for uptake by
Although
IN
supply
to
cytoplasm
1988;
also caused
probably
the
evidence,
immediately
are
Verhoeven et al.
virtual
the
by
polymeric phenolics (Manhibhushanrao
1990).
absence
of
protection given by
al.
et
1988; Asakawa
1990).
Defence
against herbivory by secondary
(Haslam
ways
accumulate
plant
1988;
material less
tasty and
in which
of
such
compounds
produce small
can
Bernays
the
tannins and other
cell
walls
(i.e.
been
in
the
phenolics
are
cells
&
is
plants
were
The
grown
may be
peat
Mole
a
a
attributed
their
as
the
and
the
bivalent
capacities
Sphagnum
This has
(Clymo
two
the
cations,
compound
of peat
of
the
lites
©
treated in
1997
Royal
as
much
layers
as
a
more
growth
1991).
Mg
2+
impregnated
for the
All
and,
very
Sphagnum
to a
smaller
+
gives
El
ions
the peat
It
has
concentrated in
been
the
high peat
(Clymo
mosses an
environment,
1982).
result of this
sativum
and it acidifies
found that
upper part
moss
1983a;
efficient
CEC
the
of the
(Botch
&
1983b).
bog ecosystem
dominance of
such
are
Hayward
&
and
against
4
effects: it
those
responsible
1983,
2+
to
1986; Kuiters
1990).
+
important
acids
filter paper, which
wet
on
are
Ca
and NH
phenomenon
of Lepidium
particularly
(Painter
as
of
release
showed that their
grown
but
have
have been demonstrated
seedlings
sphagnan,
mosses
K
as
Clymo
particularly,
1983; Clymo
properties
very
1964;
A first main effect of the
is
water
against
phenolic
Kuiters & Sarink
trap nutrients in the nutrient-deficient bog
water
Functioning
1995),
of vascular
and
of
nature
species
plants
bivalent cations such
acrotelm than in lower peat
Masing
al.
bog
also
may
Growth
for this
causes
they
in which
Sphagnum cells,
also monovalent cations such
bog
et
defences
production
hydrophilic
+
1992).
1986).
the
of
(Swain 1977;
with control
polymeric
species investigated exchange
to
the
surroundings
allelopathic effects (Huneck & Meinunger
to
strong cation exchange
mechanism
buffer-soluble
(Rasmussen
strengthen
and
substances,
number of
The uronic acids dissolved in the
Barkman
mosses
complex
stable and
1994). Experiments
was
degree,
of
amounts
Einheilig
carpets,
of
in several studies
substrates of
walls
1971;
one
relatively
strongly suppressed compared
cell
for
unattractive
very
acid have been measured in
in
mosses
Feeney
Sphagnum
was
in the
ways
digestible parts
These buffer-soluble monomeric
further
may
they
or
The various
block the
mosses
can
which makes the
against (invertebrate) herbivory
high
effect.
sphagnum
peat
&
allelopathic
as
plant growth
on
by
slow in
1995).
Waterman &
1987;
relatively
an
around
water
of
This
1992).
substances
them suitable
slow down
the
such
to
pmol
I
(Whittaker
notoriously
Breemen
makes
to
excreted
effects
growth-inhibiting
(Van
that
different
Plants
(‘quantitative’ defence),
peat
defence
a
two
1989).
diseases.
phenolics
allelopathic
be
as
in
can occur
McKey
(‘qualitative’ defence).
makes
toxins
specific
may
Rasmussen
&
relatively large quantities,
toxins
specific
also excreted into the
herbivores and
The
of
Waterman
for the herbivores
palatable
contribute
and concentrations of up
(Rudolph
tannins in
polysaccharides),
it
reported;
phenolics
as
metabolites
plant
1989;
phenolics including sphagnorubin
herbivores. No
(vertebrate)
have
amounts
al.
et
benefits of
peat
mosses
secondary plant
in
the
water-holding capacity,
the
Botanical
previous
Society
section,
of The
i.e.
bog
the
the
Netherlands,
metabolites for
vegetation.
properties
nutrient
Acta Bot.
Apart
related
trapping
Need.
46,
to
Sphagnum growth
from
capacity,
117-130
its
secondary
physical
metabo-
allelopathic
124
J.
defence
action,
vascular
over
this
the
herbivores and
against
in
plants
peat which accumulates
litter and peat
1983b,
A
is
first
the
diseases,
give peat
a
result
of
incomplete
mosses
An
1995).
reach
finally
W.
the
LIEFVELD
consequence of
Sphagnum
decomposition.
catotelm,
rate
of
the main
are
10 m
to
does
as
spp.,
The low
thickness of up
a
M.
strong advantage
a
important
from
both in the acrotelm and in
can
AND
(Clymo
1984).
why
reason
of
use
in
1993).
The low
also
anaerobic
slow,
in
pH
breakdown process
the slow
of
composition
metabolites
in
scarce
(Swift
electron
the
al.
et
that environmental conditions
The low redox
matter.
other than
acceptors
bog environment)
metabolites. We will
and nutrient
al.
et
of the
quality
al.
et
the
to
A
1981).
&
Gosselink
low pace
second
Sphagnum litter,
in
as
which
dioxide,
Mitsch
1981;
such
oxygen,
are
lead
potentials
and carbon
contributes
DeLaune
1979;
is the chemical
secondary
is
environment also
bog
decomposition
on
slow
decomposition (DeLaune
the
decomposition
so
respiration of organic
less efficient
alternative,
nitrate, sulphate (both
results
is
decomposition
unfavourable for microbial
to
as
stored and
being
VERHOEVEN
produced mainly originates
decomposition,
why peat
reasons
A.
also Van Breemen
bogs (see
is that the litter
advantage
T.
of the
reason
particular
detail the various effects of
for
the
Sphagnum
for the acrotelm and the catotelm
recycling
separately.
In the
about
walls
acrotelm,
the
by
in
higher
the
acids and uronic
phenolic
in the acrotelm (Clymo
a
high
et
al.
buffer-soluble
1995),
been shown
& Sen
an
in
the
indicated
factor
of
as
1991, 1993;
litter
also
phenolics forming
for
containing
the
acid,
cell
wall
Heijden
for
the
litter
of peat
1994).
living plants with
(see Fig.
2,
litter.
of
peat
bacteria
such
hydrolysable
slow
decomposition
buffer-soluble
in
decay
the
Fresh
peat
(Clymo
1965,
microbial use,
will
&
so
fatty
of both
1997
Royal
in
the
acid
but
The
the
greater
1992;
Society
part
Van der
to
of The
a
of
lipid,
the
cell
the
Heijden
polymeric
are
These
the main
networks,
such
polyphenolics
of the
widely
few studies in which
compared.
also
chemical
been
Johnson & Damman
decomposition.
to
of the tannin
Botanical
were
and
phenolics,
litter has
1983b;
were
make the bulk
contribute
some
species
capitulums,
the cell walls
acrotelm is
moss
surprisingly
plants
acids which form
also
probably
As the litter ages,
©
that
Rasmussen
and
litter
sphagnum
as
(Banerjee
Verhoeven
by
Sphagnum
(Fig. 3). Although
that
there have been
tannin,
initial
extracts
for the effect.
itself.
moss
the
Sphagnum
found
was
found
Rasmussen
inhibit
may
three-dimensional networks with cell wall components
hydrocarbons
surface
in the
of homogenized
and vascular
mosses
excrete
commonly
acid
they
also
mosses
values
from Sphagnum fallax and Carex
lab. The
effect
responsible
Fig. 3), although
decomposable (Rudolph
The
where
antibiotic effect
amount
no
pH
phenolic acids
assumed
was
Sphagnum
resistance
and
unavailable for
1995).
it
were
monophenolics
sphagnorubin
living peat
the low
brought
of the cell
capacity
against Gram-positive
an
showing slow decomposition
see
exchange
phanerogam)
as
effect
small
a
responsible
the
decomposition
reason
to
water,
well
as
Carex leaves had
homogenate,
particular sphagnum
composition
but the
The
containers in the
glass
homogenized
Another
bog
inhibitory
slowed down after addition of
included in
cation
who studied the breakdown of litter
(1995),
diandra from fens
whereas
1991).
A strong indication for such
1979).
& Toth
Sphagnum,
the
(Sphagnum
have
to
is the
component, particularly sphagnum
into
the acidification
firstly influenced by
only
which contribute
Painter
1964;
of fresh
decomposition
have
dead
acids,
excreted
are
Not
mosses.
than in
living
is
decomposition
living peat
wall
litter is
1994;
resistance
not
readily
Rasmussen
suberin-like
to
as
components
coating
et
on
decay (Van
al.
the
der
polymeres will become hydrolyzed
Netherlands,
Acta Bot.
Neerl.
46,
117-130
ORGANOCHEMICAL
Fig.
3.
Weight
of either
+s)
or
Error bars
Reprinted
or
distilled
indicate SE. Values
from Verhoeven
& Toth
environment,
As
cell
walls
the
are
its
by
of
plant
of
supported by
out
where
as a
are
not
homogenate of living
of initial
percentage
Science
Ltd.,
The
parts
weight
different
significantly
from Elsevier
will
they
smaller
lost
(P<0.05).
Boulevard,
further inhibit bacterial
amounts
could take
bog
organic
and
leaching
polyphenolic
matter
from
a
these
result of
activity
(Northrup
in
becoming available
compounds
nutrient recycling
(Chapin
uptake
has been demonstrated for Arctic
The
the
time-consuming
remains
molecules such
organic
(Kielland
primarily
ecological
the environment would
bypass
so
is
trees
1995).
organic
demonstrated
was
1995). This, however,
of smaller
plants
al.
nutrient-rich
It may be that
dissolved
as
it
evergreen
et
the
cells,
autolysis.
Recently,
litter of
decomposition
immobilization than is
and leave the cells
and
of
suppression
death of the
as
fresh
content
of DON
evidence, although
water
DOP, respectively).
tannin
up
the strong
degree of nutrient
litter. After the
into the
(DON
DON
decomposition-driven
acids
fresh
decaying
large
roots
letter
permission
previous section,
much
a
still bound to the
amount
significance
if
to
phosphorus
or
controlled
be
leads
will be leached
the nutrients
same
addition of
expressed
1986).
found in
normally
cytoplasm
nitrogen
the
indicated in the
already
of the
that
into
& Sarink
the
by
are
UK.
and
released
Values
with kind
(1995),
0X5
1GB,
with
Sphagnumfallax
followed
125
SPHAGNUM
(+w).
water
Langford Lane, Kidlington
(Kuiters
IN
loss of litter of Carex diandra and
species (+c
per week.
COMPOUNDS
1994).
For the
as
to
be
amino
environ-
bog
ment, it has been found that mineralization of nitrogen is faster than would have been
expected
on
Verhoeven
the basis of the slow
et
al.
It
1990).
recycle
their nutrients in
uptake
of mineral
the
cytoplasm
a
nitrogen
after
decomposition
the
resistance
©
Royal
Botanical
rates
(Waughman 1980;
probable
that
the
peat
faster way than
normal, possibly by uptake
which has been
quickly
moss
the further
strong
most
released
by
Damman 1988;
mosses
in
of DON,
bogs
or
by
microbial breakdown of
autolysis.
The influence of peat
1997
decomposition
is, therefore,
secondary
of Sphagnum
Society
metabolites in the catotelm is
and humification of the
of The
litter
to
Netherlands,
plant
decomposition
Acta Bot.
Need.
totally
related
to
material. Further evidence for
46,
was
found
117-130
by
Coulson &
126
T.
J.
A.
VERHOEVEN
Butterfield (1978),
who detected that the remains of peat
still
intact
much
more
still
be present
The
main
bog
and
into the
bog
catotelm
almost
acid
sphagnum
as
of the
before
in
in
do
they
the
It
plant
properties.
carbonyl
acid,
core
phenolic-derived
play
not
role here,
a
reach
can
have
animal
the
their
through
FINAL
high
to
and
a
effect
tanning
The
remains,
CEC
this
These
themselves
The great
1).
aquatic
the humic
these
compounds
peculiar
nutrients in
an
in
the
to
the
& Painter
its
do
tanning
tanning
reactive
of 5-keto-Dmolecule
acids
1983,
the usual
These
and
1991).
In
aromatic,
humic
acids
molecules and
highly refractory
is
as
many
amino
(Painter
not
is
have
polymeric
proteins,
are
cell walls
strong
not
residues
are
bodies,
glycuronglycan,
Sphagnum
polysaccharides.
their
also
1984).
above,
appears
as
well
of
variety
as
the role of
to
organochemical compounds produced by
be of great significance, for the performance of the
for the
functioning
bryophytes.
blocks of
sphagnum
the cell walls the
of the cell wall chemical
acid and
rigidity
gallic
necessary
give
the
peat
to
mosses
compounds
and uronic acids,
are
acid and
properties
impregnated
large
attack and
well-known
for the
with
a
a
cation
whole
moss
cell
functioning
of
build-
lipoid coating, gives
water-filled
herbivory.
high
related
to
©
not
secondary
the
1997
associated
more
likely
to
with
leach
effects which favour
allelopathic
The influence of the
primarily
as
The
hyaline cells,
polymeric
exchange
and
unronic
capacity,
which
capture and hold metals and nutrients in their extremely nutrient-poor
environment. The
and may have
their
bog ecosystem
phenolic network, including
for the mosses’
provides protection against microbe
enables them
of the
substances associated with the peat
secondary
The three-dimensional polymeric
are
to
human
contains
humic acids
these
phenolics
and
REMARKS
mosses
acids
it
groups
sphagnan
importance
also
as
exert
can
because
walls indicates the
ing
hydrolysable
substance
including
polysaccharides
respect
of
binding
(Smidsrod
Sphagnum representatives
(Table
down in
proteins
on
main
from the
water, where it
Normally,
side chains.
but
other
to
the peat ages and leach
as
which constitutes about 25% of the
substances for
From the studies discussed
peat
stable
very
break
they
as
catotelm. The
1994).
autohydrolysis
the formation of
structures
nitrogen
sequester
the
The
1991).
lead
can
case, the
the
may
1994).
in the catotelm contribute further
water
Heijden
and
bog
in
unique
compound
a
(Painter
polypeptides
this
is
the
amines.
groups in
(C-O-C)
sphagnan
and
Sphagnan
mannuronic
into
leaches
proteins
on
is
Heijden
strong tanning properties of bogs, which have led
holocellulose
through
peat ages.
influence
der
against decomposition
they
der
(Van
of
perfect preservation
released
were
immediate
Sphagnum peat
(Van
sphagnan (Painter 1983). This polymeric uronic acid, also known
slowly
their
and the humification of the peat. The soluble
where
catotelm,
for the
responsible
LIEFVELD
hydroxybutenolide through peroxidative degradation,
to
microbes
on
M.
deep peat layers
plants
walls, however, become partly hydrolyzed
water
effect
inhibitory
bog
70 000 years old
are
bog
decomposition
decomposed
tannins in the cell
in
mosses
wall polysaccharides
resistance
strong
available in the
of the
such
further
which
other
W.
mentioned above.
of the acrotelm
water
are
the
becoming
very slow pace
monophenolics
the
for
of
stems
the cell
deep peat layers
network
Substances
the
in
reason
polyphenolic
the
fact, the bulk of
In
surroundings.
than
AND
metabolites
decomposition
Royal
Botanical
the
out to
cell
the
Sphagnum
on
the
wall,
bog
of The
as
monomeric
in the acrotelm,
spp.
functioning
of the
of litter and peat. The
Society
such
water
Netherlands,
bog ecosystem
constant
Acta Bot.
addition of
Neerl.
46,
117-130
ORGANOCHEMICAL
of
the environment
to
protons
degradation
decomposition
products
and
by
in
the
the
which is caused
the release of
catotelm is
by
down
result
of all
carbon storage function of
peat
important
and tannins and
compounds
it
can
is
bogs
recalcitrant
production
The
nature
rate
of
of dead
metabolites associated with the cell
acrotelm,
these
slow. Hence,
extremely
very
and
exchange
environment.
bog
the
by
secondary
in the
cation
acids,
acidic
typical,
the
phenolics
a
127
SPHAGNUM
being slowed
catotelm environment. As
rate
IN
excretion of
through
creates
is further
Sphagnum tissue,
walls,
COMPOUNDS
to
a
together,
be
in the
sphagnan
the
decomposition
concluded that
the
globally
associated with the
large degree
suite of secondary plant metabolites produced by the main peat-forming plants, the peat
mosses.
SUMMARY
The
bryophyte
chemical
most
and
metabolites
their
to
ecosystem
The
which
properties
reference
as
a
ecological
but
such
carbohydrates,
also
in
of the
are
in
capacity,
in
the
cell
enables them
in the
death
of the
cells.
breakdown of all cell wall
layers
tannins in
in
the
for
water
on
effect
and
with
for
of
special
the
bog
the
on
of
have
a
tanning
acid
be
(p-hydroxy-(ifor this
together
acid,
can
phenolics,
genus
is present in the
group of
needed for the
in
a
any
defence
with
other
compounds
which
also
are
form
peat
mosses
large water-holding
herbivores and
against
systematic
may have
The monomeric
way.
functions. The
allelopathic
their
of the
functioning
and
high
cation
on
bog ecosystem
which is of
excreted in the
bog
recycling of nutrients
in
the
and this
The
effect
here
the
are
specific
networks,
second
provide
cell
walls
protective
polymeric
deep peat layers. These tannins, together
catotelm,
which is
decomposition,
phenolics
years.
sphagnum
galacturonic
as
monophenolics
acrotelm,
The
discussed
compounds
exchange
bind metals and nutrients.
polysaccharides,
thousands
The
rigor
and
the
give
firmly
to
for the peat storage function. The
peat
further fate
reviewed,
associated with the cell walls.
investigated
bog
walls
inhibitory
decomposition
such
also will
been
The effects of these metabolites
the
in
and
physical
unfavourable for
far. This phenolic
so
polymeric
walls.
‘sphagnan’,
They
not
into
the
associated with their
after
component
have
and
plants
Sphagnum
of which is
the cell walls the
give
by
studied
the cell
named
cells.
excreted
which
microbial
and
are
Sphagnum
monophenolic
a
uronic acids
particular
in
This is
three-dimensional
hyaline
acids
polyuronic
to
production
group of
major
representatives
diseases, although this has
phenolics
the
produced
important
most
gallic acid,
as
polymeric phenols
capacity
vegetation
known
acidic
wet,
the
paper,
for
significance
acid).
large polymeric molecules,
The
this
groups. A first
the
metabolites,
fluids
In
compounds
two
and has been found in all
cell
mosses are
produced by Sphagnum representatives
(carboxymethyl)-cinnamic
phenolics
dominant
a
whole.
divided into
secondary
as
their environment
keep
microbes.
organochemical
roughly
occurs
and fens worldwide. The peat
higher plants
secondary
Sphagnum
genus
peat-forming bogs
with the
proteins
water
is
sphagnan
slow down
the
prohibit
of
mostly
relatively rapid
action may
networks
are
great importance
microbial
persist
phenolics
in
deep
release
which is released
and further slow
down the
peat
decomposition.
ACKNOWLEDGEMENTS
This paper
Western
©
1997
was
written
during the first author’s stay
Australia, supported by
Royal
Botanical
Society
of The
the Netherlands
Netherlands,
at
Murdoch University, Perth,
Organization
Acta Bot.
Neerl.
46,
for Scientific Research
117-130
J.
128
and
(NWO)
comments
Murdoch
by
and
hospitality,
to
to
Dr E.
earlier
an
We
University.
der
van
are
Heijden,
draft of this
T.
A.
VERHOEVEN
indebted
AND
M.
W.
LIEFVELD
Prof. Dr A. J. McComb for his
to
Dr R. Aerts and Dr G. Niemann for valuable
manuscript.
REFERENCES
T.V. &
Armentano,
in
change
wetlands
the
E.S.
Menges,
carbon
of the temperate
Patterns
(1986):
balance
of
zone.
J.
Ecol.
of
lation
carbon
lands
SPB
of wetlands
and
nitrogen.
and Shallow
Academic
Y.
Asakawa,
(1990);
with
bryophytes.
In:
(eds):
B.C.
(ed.):
Water Bodies-.
The
Their
369-410.
aromatic
from
chemistry
Clarendon
&
carbon
and
chemical
In:
cycle theory.
H.
M.L., Konings,
&
SPB
the
carbon/
T.L.
Pons,
in
R.S.
Clymo,
the
of
in
of
&
S.P.
Sen,
J.J.
Barkman,
(1992):
of
and
bogs
The
the
R.S.
Phil.
and
in
Bogs
heath
R.S.
Clymo,
and
syn-
in
The
(ed.):
Fens
pools
J.T.A.
The Netherlands:
Kluwer
Academic
conservation:
Publishing,
159-224.
neglected
of
component
decomposability—a
fitness. J.
plant
Ecol.
and
G.
&
and
plant
the
Bilgener,
tannins.
Adv.
World:
Brinson,
Ecol.
Brown,
of
95-152.
Ecol.
Res.
D.H.
12:
&
inorganic
R.
chemical
in
In:
wetlands.
S.
(1990);
In:
bei
(1981):
&
Meema,
Pollutants
on
513-
Ann.
Cellular
Their
299-318.
Rev.
uptake
H.D.
chemistry
Clarendon
&
Royal
A.J.E.
Chapman
J.P. &
230:
(1982):
P.M.
Smith,
&
and
The
(ed.):
ecology
Bryophyte
London.
Hall,
Chapin III,
F.S.
(1985):
antiherbivore
plant
895-899.
Butterfield,
ofthe biotic factors
F.
den
J.
(1978):
An
investi-
determiningthe
blanket
on
Zur
(1899):
Laub-
und
Czapek,
F.
bog.
J.
rates of
Ecol.
66:
Chemie
der
Lebermoosen.
Zellmembranen
Flora
86:
361-
removal
other
and
Press,
and
Botanical
Society
of The
(1988):
R.D.,
bei
Oikos
51:
Reddy,
matter
Netherlands,
Regulation
in
retention
peatlands.
DeLaune,
Zellmembranen
Moosen
und
Jena.
A.W.H.
Damman,
&
(1913):
Fischer,
(1981): Organic
1997
Berlin.
con-
Oxford.
©
with
Sphagnum
T.C.
381.
and
Zinsmeister,
(eds): Bryophytes.
taxonomy:
Science
Farnen.
J.M.
303: 605-654.
of
631-650.
123-161.
Wells,
peat bog growth.
B
Agricultural Systems:
Hayward,
plant decomposition
the
of
Czapek,
Brown,
decomposition
chemicals.
Amsterdam.
to
Land.
availability
J.C.
gation
Mires:
(ed.):
Ecosystems
&
freshwater
(ed.):
Ecosystems of
19:
Amsterdam.
A.E.
productivity,
activity
Moor.
Elsevier,
A.J.P.
Gore,
Hutchinson,
and
229-289.
(1989):
Mire ecosystems
A.P.A.
Gore,
and
M.M., Lugo,
Syst.
Mues,
In:
Fen
Bog,
Primary
sumer
Masing, V.V. (1983);
USSR.
Swamp,
In:
Elsevier,
Soc.
In:
Sphagnum.
Resource
M.
263-302.
in
air.
R.S. &
Coulson,
M.S. &
some
849-869.
and Moor.
Interactions
(1987):
Wetlands
defense.
Herbivores
Botch,
Royal
Coley, F.D., Bryant,
E.A., Cooper,
747-757.
Sphagnum,
(eds): Effects of Atmospheric
Ecology:
82:
187-190.
Bernays,
of
Ecol. 61:
The limits
Springer Verlag,
Clymo,
Dordrecht.
Litter
(1994):
the break-down
173-236.
of
F.
Berendse,
on
vegetation, history,
530.
and
J.
in
acidity
141-153.
communities
Verhoeven,
dynamics
and
53:
growth
Fen
Bog.
(1984):
Trans.
Forests,
nutrient
nitrogen
67: 427-^431.
Ecol.
Peat.
(1983b):
Swamp,
World:
Clymo,
K.M.
In:
Netherlands.
The
(1983a):
R.S.
Clymo,
water
ecology
the
Rate'.
Publishing,
82:
Plant
large
Causes
(eds):
Growth
(1979); Antibiotic activity
bryophytes. Bryologist
aspen
for the
in
cog
origin
J.
bogs.
Hague.
Banerjee, R.D.
The
effects of environment.
Mires:
Academic
leaves
(1965): Experiments
R.S.
quaking
199-200.
(1964);
Sphagnum
Clymo,
Lambers, H., Cambridge,
Variation
Consequences of
313-340.
of
their
chem-
secondary
of
New
(1995):
377:
Sphagnum bogs. Bryologist
for
consequences
R.S.
Clymo,
value
P.B.,
Effect
(1987):
513-517.
F.S.
Nature
cycle.
Oxford.
Press,
Introduction
budget.
nutrient
and
significance
R.
Mues,
re-
(Choristoneura conflictana (Walker)).
73:
Oecologia
Chapin III,
in
Reichardt,
R.A.
Michx.)
tremuloides
(Populus
T.P.,
Werner,
nutritional
(1983):
plants
Oikos 40: 357-368.
herbivory.
&
D.R.
Klein,
boreal
fertilization upon the
nitrogen
and
of
Clausen,
M.C.
aspen tortrix
(1989): Secondary plant compounds,
WJ.
ecological
of
istry
281-311.
and
H.D.
Zinsmeiter,
of
Hague,
Terpenoids
J.P.,
McCarthy,
Wet-
pharmacological activity
Bryophytes.
taxonomy.
and
Coastal
The
(1990):
global cycles
Patten,
Publishing,
compounds
the
to
In:
J.T.A.
balance
to vertebrate
Bryant.
Verhoeven,
T.V. &
contribution
Baas,
Carbon/nutrient
74: 755-
774.
Armentano,
F.S. &
Bryant, J.P., Chapin III,
soil-
organic
of
Sphagnum
nitrogen
bogs
and
291-305.
C.N.
&
Patrick,
decomposition
Acta Bot.
Need.
in
46,
W.H.
soil
as
117-130
ORGANOCHEMICAL
influenced
and redox
by pH
Biochem.
conditions.
IN
SPHAGNUM
Soil Biol.
13: 533-534.
H.J. & Van
During,
COMPOUNDS
interactions
other
B.F.
(1990): Bryophyte
Bol.
plants.
J.
Linn.
Soc.
F.A.
action
of
Tang,
C.S.
188.
Mechanisms
(1986):
allelochemicals.
and
modes
of
A.R.
&
Putnam,
171-
of Allelopathy.
Chichester.
B.
Millon’s
In:
The Science
(eds):
Wiley,
Engmann,
der
mit
Substanzen
der
Untersuchungen
anfarbbaren
Reagens
Biochem.
Physiol.
Pflanzen
163: 200-215.
flavonoids
&
from
R.
Mues,
Phenolic
(1990):
J.
chemical
In:
bryophytes.
than
Zinsmeiter,
H.D.
Their
(eds): Bryophytes.
171-207.
taxonomy.
other
compounds
and
chemistry
Clarendon
Press,
Oxford.
carbon
Northern
(1991):
and
cycle
Ecol.
wanning.
Haslam,
peatlands:
role
responses
to
possible
1:
Appl.
and
tannins)
chemical
in
the
in
defense.
132:
Chem.
J.
Their
289-298.
H.A.P.
Elsevier,
14:
and
K.
contribution
&
in
in
V.
of
Bryo-
taxonomy:
leaves
In:
Gore,
A.J.P.
A.W.H.
(1991): Speciessouth
a
Swedish
Biochem.
A.W.H.
(1993): Decay
Adv.
Amino acid
for
Ecol.
plant
78:
absorption by
arctic
nutrition
nitro-
and
2373-2383.
Phenolic
Sarink,
H.M.
from
and
Poorter,
causes
Res.
Royal
and
PhD
T.J.
Lindow
bodies:
23:
S.
Rasmussen,
the
and
plant
dissertation,
(1986): Leaching
leaves
(1992):
and
needles
Soil
trees.
Inherent
higher plants:
ecological
of
of
Biol.
a
variation
search
for
consequences.
with
cell
&
Rudolph,
of The
Netherlands,
Tollund
wall
of
and
Cell
Wall
142.
Meeting'.
sequestering
123-142.
Do
in
serve
Sassen,
and
reactive
a
15:
(1992):
Sphagnum
man
preservative
sphagnan,
H.
hu-
aquatic
124: C22-C26,
man,
tanning
Vogt,
nitrogen
227-229.
of
Res.
the
&
phenolics
function
a
M.M.A.
University
(ed.):
Press,
Nijmegen.
S„
C.
Wolff,
&
Rudolph,
Compartmentalization of phenolic
G.A.
H.
Rudolph,
The
(1986):
Sci.
higher plants.
Am.
chemical
254:
(1995):
in
Biochem.
defenses
of
76-81.
Identifikation
(1972):
H.
constituents
38: 35-39.
Sphagnum. Phytochemistry
der
Czapekschen
Physiol. Pflanzen
163:
110-112.
H.-J.
Rudolph,
Bat.
&
Ges.
80:
des
&
Crypt.
H. &
of
Bot.
Samland,
of
H.
Smidsrod,
J,
Int.
O. &
from
Neerl
Dtsch.
46,
Studies
on
cultivated
Occurrence
acid
the cell
in
in
and
walls
of
24: 745-749.
of northern
Environ.
T.J.
peatlands
balance
Sci.
7:
of the
11-14.
Contribution
of
of
(1984):
peat-bog
127: 267-281.
801.
Ergeb-
cation-exchange selectivity
Painter,
humus
(1992):
for the carbon
J. Ecol.
to the
Acta
Her
(1985):
zonation
importance
carbohydrates
aquatic
Neue
3: 67-73.
sphagnum
(1981): The
and their
S.
Sphagnum
bryophytes. Phytochemistry
Sjdrs,
(1967):
Sphagnols.
Rasmussen,
metabolism
bioreactors.
B.
114-118.
H.J.
Rudolph,
Engmann,
Konstitution
zur
Rudolph,
Res.
187-261.
Society
of
content
European
of
Carbohydrate Polymers
atmosphere.
and
action
glycuronglycan
in
R.A.
Nature 377:
(1991):
antimicrobial
in
litter.
peat-bog
metabolism
coniferous
H.
Botanical
pine
Oxford.
control
peat. Carbohydrate
other
secondary
acids
ecosystems.
rate between
physiological
from
R.
chemical
575-579.
Z., Dahigren,
Polyphenol
Mues,
mineral
(1983): Carbohydrate origin
from
mus
nisse
18: 475-480.
H. &
growth
(1995):
75:
Oecologia
ecosystems.
&
Press,
and
decomposition
Northrup, R.R., Yu,
Sphagnolkristalle,
Amsterdam.
deciduous
influences
Rasmussen,
and Moor: 67-220.
on
Phenolic
for
different
at
and
chemistry
Clarendon
436.
—
(1988):
of flavonoids
taxa
Zinsmeiter, H.D.
6th
(eds):
Sphagnum peatlands.
(1987):
forest
421
taxonomy.
Nicolai,
Wetlands
York.
bryophyte
Their
Bryophytes.
Rosenthal,
phenolic compounds
Lambers,
In:
(eds):
23: 103-114.
(1993):
New
R.
chemical
Fen
Damman,
(1994):
A.T. &
several
taxonomic ranks.
disease resist-
Hung.
significance
of
N.
Matsuyama,
plant
J.G.
similar to that of lignin ? In:
Oxford.
Press,
Damman,
University,
Kuiters,
©
and
a
growth
The
(1990):
and
in
and
Regional
27: 999-1023.
M. &
and liverworths.
Mues,
Swamp, Bog,
A.T.
growth
1997
mosses
&
cycling. Oecologia
Kuiters,
Adv.
of
(1983): Hydrology.
plants: implications
in
bryophytes,
H.D.
regulation
Kielland,
Free
Plant
5: 249-296.
Bryol.
gen
Am.
Oikos 61: 234-242.
L.C.
its
The
metabolites
ecosystems.
(1990):
Sphagnum decay
bog.
Johnson,
(1988);
Amsterdam,
controlled
raised
L.
chemistry
L.C. &
Johnson,
of
Clarendon
Mires:
(ed.);
R.G.
terrestrial
ecology
Zinsmeister,
Ingram,
R.
classification
the
properties.
acitivities
to the chemical
phytes.
Cates,
Meinunger,
&
regulatory
In:
soils.
Entomol.
Phytopathol.
Reinhold,
Painter
Ecol.
metabolism
Van Nostrand
Mues,
ecological
an
157-176.
wetland
Gosselink,
vegetable
869-883.
S.
other
W.J. &
release
plant secondary
in
decomposition
Huneck,
Acta
Painter,
J.R. &
of carbon-based
Nat.
ance.
K.A.
1789-1806.
Horner, J.D., Gosz,
role
phenolics:
105:
Immirzi, P. (1993): Carbon dynamics
and
Phenol
(1988):
global
182-195.
(1988): Plant polyphenols (syn.
E.
Am. Nat.
Manhibhushanrao, K., Zuber,
forest
E.
Gorham,
&
peatlands
Mitsch,
(1972):
Sphagnenzellwand.
Gorham,
Maltby, E.
Plant
(1971):
global perspectives. Chemosphere
104: 79-98.
Einheilig,
D.A.
Levin,
perspective.
Tooren,
with
129
117-130
water.
Carbohydrate
130
J.
P.
Swain,
(1977): Secondary compounds
tive
agents.
Swift,
M.J.,
Ann.
Plant
Rev.
O.W.
Heal,
in
(1979): Decomposition
R.
&
kristallinen
num
Phenols
mageltanicum.
(1973):
aus
der
Van
Struktur
Zellwand
Dtsch. Bo I.
eines
von
eines
P.H. &
grown
and
Phenols
In:
164:
How
E.
Heijden,
pyrolysis
(1994):
A combined
spectrometric study
mass
PhD
tissues.
plant
down
dissertation.
der
Phenolic
Rudolph,
H.
Boon, J.J.,
(1997): Sphagnum
Waughman,
of peatified
ecology
Rasmussen,
of
kers
for
fossilised
Biomolecules,
Verhoeven,
in
fens
and
bogs.
in
as
peats.
J.
E.
&
phosphorus
Ecol. 78:
Toth,
E.
&
biomar-
©
Schmitz,
Wilschke,
of
(1989):
Herbivory
rain-forest
M.J.A.
plants.
(eds):
Tropical
536,
Elsevier,
(1994):
Mole,
M.B.
Analysis
Blackwell
of
Scientific
Oxford.
Chemical
(1980):
South German
R.H. &
Feeney,
P.P.
interactions
J.,
Hoppe,
of
aspects
peatlands.
(1971):
between
Mues,
and chemical
E.
&
of
J.
the
Ecol.
Allelochemi-
species.
R.
Science
253-263.
(1990):
Zinsmeister,
In:
acid.
(eds): Bryophytes:
taxonomy:
H.-J.
Rudolph,
sphagnum
their
chemistry
Oxford
Science
Publications, Oxford.
Wilson, M.A., Sawyer,
in fens; effect of litter
Botanical
S.
Metabolites.
some
Biosynthesis
mineralization in
Royal
in
171: 757-769.
(1995): Decomposition
1997
D.
157-160.
&
G.J.
cals: chemical
Ancient
713-726.
Sphagnum litter
stable
66:
1025-1046.
H.D. &
Maltby,
and
J.T.A. &
of Carex and
Sphagnum
S.
press.
J.T.A.,
(1990): Nitrogen
Verhoeven,
68:
and its decar-
boxylation product isopropenylphenol
plants
with
513
P.G.
anatomical
University
acid
of
growth rates
Ecosystems'.
Plant
Whittaker,
Heijden, E.,
Werger,
S.,
composition
McKey,
&
Forest
Waterman,
10: 270-
Amsterdam.
Van
H.
Lieth,
Larsson,
Arwidsson, E., (1985):
Oecologia
&
homogen-
Amsterdam.
Sphagnum bogs
(TREE)
P.G.
tissue
A.J.S.,
&
chemical
nutrition.
Publications,
der
and
in
LIEFVELD
271-275.
McDonald,
A.
M.
living
27:
secondary compounds
Rain
461—464.
W.
by
Biochem.
at constant relative
Waterman,
Kreher,
275.
Van
inhibition
Biol.
R.H.,
mineral
Sphag-
Ges. 6: 309-311.
AND
Ericsson, T., Wiren,
Sphagnum magellanicum.
Trends Ecol. Evol.
plants.
von
kristallinen
Physiol Pflanzen
Breemen, N. (1995):
other
Waring,
Ecosystems.
(1971): Isolierung
der
aus
Ber.
Zellwand
Biochem.
and
Soil
ates.
Dilferences
H.
Rudolph,
Tutschek, R., Rudolph, H„ Wagner,
R.
J.M.
Anderson,
Terrestrial
VERHOEVEN
quality
protec-
as
Oxford.
Blackwell,
Tutschek,
A.
28: 479-501.
Physiol.
&
T.
Society
E.
(1989);
mosses.
of The
J.
Hatcher,
P.G. & Lerch
1,3,5-hydroxybenzene
Phytochemistry
Netherlands,
28:
structures
111,
in
1395-1400.
Acta Bot.
Neerl.
46,
117-130