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LIGNOTUBERS IN SEQUOIA SEMPERVIRENS: DEVELOPMENT AND ECOLOGICAL SIGNIFICANCE
Author(s): Peter Del Tredici
Source:
Madroño,
Vol. 45, No. 3 (JULY-SEPTEMBER 1998), pp. 255-260
Published by: California Botanical Society
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Madroño,
Vol.
45,
No. 3,
pp.
255-260,
1998
LIGNOTUBERS IN SEQUOIA SEMPERVIRENS : DEVELOPMENT AND
ECOLOGICAL SIGNIFICANCE
Peter Del Tredici
The Arnold
Arboretum of
Harvard
University,
125 Arborway,
Jamaica
Plain,
MA 02130, USA
Abstract
Seedlings
of
Sequoia sempervirens
(D. Don)
Endl.
develop lignotubers
as
part
of their
normal
ontogeny
from detached
meristems
located in the axils of
the two
cotyledons.
Within four
months of
germination,
each
axillary cotyledonary
meristem
gives
rise to a
large
central bud with two
or more
collateral
accessory
buds. As
seedlings age,
bud and
cortex
proliferation
phenomena
associated with
lignotuber
formation
spreads
distally
to include
axillary
meristems
located
immediately
above the
cotyledonary
node.
Ligno-
tubers continue to
expand throughout
the life of a
Sequoia,
eventually
forming
massive,
basal
swellings
that are covered with
leafy
shoots
and/or
suppressed
shoot
buds. The
Sequoia
lignotuber
is
a
specialized
organ
of
regeneration
and
carbohydrate
storage
that
contributes to the
long-term
survival of
the tree
by
producing
buds that
can
develop
into
shoots
following
traumatic
injury
to
the
primary
trunk
and
by
generating
new roots that
increase the
stability
and the
vigor
of both
young
and old
trees.
In
response
to
a variety
of
exogenous
factors,
Sequoia
will
also
produce
induced
lignotubers,
or
burls,
on
the trunks of
mature trees as well
as on the
"layered"
lateral
branches
of
young
trees,
where
they
come
in
contact
with the soil.
The
California coast
redwood,
Sequoia semper-
virens
(D. Don)
Endl.
(Taxodiaceae (henceforth
re-
ferred to
as
Sequoia)),
is famous not
only
for
being
one of the
tallest trees in the world
but also for its
ability,
unusual
among
conifers,
to
resprout
vigor-
ously
after
being
cut
down. While much
has been
written
about the
commercial and
ecological
im-
portance
of
resprouting
in
redwood
(Olson
et al.
1990),
little is known about
the
precise origin
of
these
sprouts,
which arise from
a large
"burl" lo-
cated at
the base of
the tree
(Becking
1968;
Stone
and
Vasey
1968;
Simmons
1973;
Groff and
Kaplan
1988).
There are
numerous
reports
in the
literature of
woody
plants
that can
resprout
from
underground
burls,
technically
known as lignotubers,
following
traumatic
injury
to the
primary
trunk.
Anatomical
studies on
several arborescent
taxa,
including
Eu-
calyptus
spp. (Carr
et al. 1984),
Arbutus
unedo
(Sealy
1949),
Quercus
suber
(Molinas
and
Verda-
guer
1993),
and
Ginkgo
biloba
(Del Tredici
1992,
1997),
have shown
that
lignotubers
are
genetically
determined
structures that
develop
from buds lo-
cated in the axils of
both
cotyledons
and a few of
the
leaves
immediately
above them.
Over
time,
lig-
notubers
can become
quite
large
and
contribute
to
the
survival of
plants
in
three
ways:
1) they
are a
site for the
production
and
storage
of
suppressed
shoot buds
that can
sprout following
injury
to the
primary
stem;
2) they
are
a site for the
storage
of
carbohydrates
and mineral
nutrients,
which
may
al-
low for
the
rapid
growth
of
these
suppressed
buds
following
stress or
damage;
and
3) for
plants
grow-
ing
on
steep
slopes, they
can
function as a kind of
clasping organ
that
anchors the tree to the
rocky
substrate
(Sealy 1949;
James
1984;
Del Tredici
et
al. 1992).
Lignotuber-producing
species
are most
common-
ly
found in
Mediterranean-type ecosystems
that are
characterized
by hot,
dry
summers
and periodic
fires
(James
1984;
Mesleard
and
Lepart
1989;
Can-
adell and
Zedier
1994).
The
purpose
of the
present
study
is twofold:
first,
to determine
whether or not
the basal
swellings
produced by Sequoia
fit
the def-
inition
of an ontogenetic lignotuber
(Carr
et al.
1984;
James
1984;
Canadell and
Zedier
1994),
and
second,
to
examine the
ecological
role
that these
structures
play
in the
tree's native
habitat in the
coastal
forests of northern
California.
Materials and
Methods
Seeds of
Sequoia sempervirens
were extracted
from
green
cones collected from
the
ground
in
Richardson
Grove State
Park,
Humboldt
County,
California,
on 28 October 1993. The cones had
been
dislodged
from trees
by squirrels feeding
in
the tree
crowns. Cones were taken to
the Arnold
Arboretum in Boston, Massachusetts,
where
they
were allowed
to air
dry
until
they
shed their
seeds.
These were
sown
in
a warm
greenhouse
(heated
to
a minimum
temperature
of
17°C)
on
29 November
1993
and
13
April
1994.
For
both
dates,
germina-
tion
commensed about two
weeks later. A
minimum
of
ten
undamaged seedlings
were
sampled
at each
of four time
periods:
15, 37, 59,
and
133
days
after
germination.
At
the time of
sampling,
two
to
three
mm
long segments
of
the
primary
axis,
including
tissue
above and below the
point
of
attachment
of
the
cotyledons,
were collected from
the
plants,
fixed
in
FAA,
dehydrated
in
a
t-butyl
alcohol
series,
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256 MADROÑO [Vol.
45
and
embedded in
paraplast.
Serial
transections,
10
microns
thick,
were cut on a rotary
microtome and
stained with
Heidenhain's
hematoxylin
and safranin
(Johansen
1940).
For the
purpose
of
studying
the
later
stages
of lignotuber
development,
a dozen
three-year-old
redwood
seedlings
were
purchased
from
a California
nursery
and cultivated
in con-
tainers
in the
greenhouse
for three
years.
Observations
on mature
Sequoias
, both
logged
and
unlogged,
were made
during
October
1993,
at
four sites in
northern
California:
Redwood National
Park and
Humboldt Redwoods State
Park in Hum-
boldt
County, Big Basin Redwoods State Park
in
Santa
Cruz
County,
and Samuel
P.
Taylor
State
Park
in Marin
County.
Seedlings
of
Sequoia, mostly
one
to four
years
old,
were collected on 26 October
1993,
along
with a few
small
layered
branches from
older
Sequoia
saplings.
Both the
seedlings
and the
layers
were
brought
back to the Arnold Arboretum
for further
study
and documentation.
At the same
time,
numerous "live burls" were
purchased
from
tourist
shops
located near Redwood
National Park.
These were
placed
in shallow dishes
of water in a
warm
greenhouse
heated
to a minimum
temperature
of 10°C.
Results
Lignotuber
development
on
seedlings:
15
to 180
days.
Observations
on
greenhouse-grown
seedlings
indicate that
lignotubers
in
S. sempervirens
origi-
nate
from
exogenous
meristems
located in the axils
of the two
cotyledons.
On
15-day-old
seedlings,
the
axillary cotyledonary
meristems
are
poorly
differ-
entiated,
being
little more than a single,
superficial
layer
of meristematic cells
approximately
0.3 mm
across,
with
no vascular connection to the stele
(Fig.
1).
By
37
days,
structures
identifiable as mer-
istems
develop
in the axils of the
cotyledons,
but
their vascular connection
to the stele is only par-
tially complete.
By
59
days,
the
axillary cotyledon-
ary
meristems
produce
foliar
primordia
and estab-
lish a complete
vascular
connection to the stele
(Fig. 2). By 133 days,
the
axillary
cotyledonary
meristems
develop
into distinct buds that
protrude
from the
stem
by
as much as 0.5
mm,
and collateral
accessory
buds
develop
adjacent
to
the
primary
cot-
yledonary
bud
(Fig.
3). By
the
time
seedlings
are
six months
old,
clusters
of buds are
readily
visible
at both
cotyledonary
nodes,
with
some
of
them
pro-
ducing
vegetative
shoots.
Lignotuber development
on older
seedlings
: one
to
five
years.
On 3
to
5-year-old
collected
seedlings,
the
cotyledonary
node
is
readily
identifiable
by
the
oppositely
arranged
pair
of
protruding
bud-clusters
at the base
of
the
stem.
Depending
on the
vigor
of
the
seedling
and the amount of
damage
it has sus-
tained, one, both,
or neither of the
cotyledonary
bud-clusters were
producing leafy
shoots,
0.5
to
4.0
cm
long
(Fig.
4). While
sprouting
is common in
seedlings
that have
experienced damage
to the
pri-
mary
stem,
it also occurs in
seedlings
that showed
no
signs
of
injury.
In addition to shoot
production,
the
cotyledonary
node
region
of the collected seed-
lings
often
produce
adventitious
roots in
response
to
partial
burial.
Typically,
wild-grown Sequoia seedlings
do not
develop
visible bud
swellings
at the
cotyledonary
node until
they
are between three and
six-years-old
(Becking
1968;
Simmons
1973).
In contrast,
lig-
notubers
of greenhouse-grown seedlings
produce
abundant bud clutsters and/or
sprouts
by
the time
they
reach one and a half
years
old. After four or
five
years
of
cultivation,
the cortical
swelling
and
bud proliferation
associated with
lignotuber
for-
mation
spreads
distally
to
engulf
many
of the nodes
produced
during
the first
growing
season
(Fig.
5).
Lignotuber
development
on mature trees.
Lig-
notubers
expand
throughout
the life
of
a Sequoia
,
eventually
forming
a massive,
woody swelling
at
or
just
below
ground
level. The outer
surface
of
this
swelling
is
generally
covered with shoot buds.
On
undamaged
trees,
lignotubers
typically
give
rise
to clusters of small
leafy
shoots
encircling
the
base
of
the trunk. On trees
damaged by logging
or ero-
sion,
lignotubers give
rise to
large secondary
trunks
that
equal
or exceed the
primary
trunk. Mature trees
that
had been
logged
90
to
100
years
ago
have now
developed
lignotuber
sprouts
well over a meter in
diameter. When
second-generation
trees are found
growing
on a steep slope
near
a stream or a road
cut,
the
woody
lignotuber
is readily
observable as
a massive
"plate"
of
downward-growing
tissue that
follows the contours
of the
ground
and extends two
to three m out from the
nearest trunk. As well as
giving
rise to new
shoots,
such
exposed
lignotubers
are
also the source of roots that
help
to anchor trees
to
eroding
slopes
(Fig.
6). On
rocky
sites,
the
lig-
notuber has a tendency
to form a kind
of
clasping
organ
that
envelops
the
adjacent
substrate,
further
stabilizing
the tree.
Induced lignotuber development
on layered
branches. Induced
lignotubers
were observed
to
de-
velop
on the
layered
branches of
29-year-old
Se-
quoia
saplings,
the
growth
of which was limited
by
low
light
levels that
prevail
beneath
a mature red-
wood forest
canopy.
The stems of these
plants
are
typically
weak
and
spindly,
and,
when
pinned
down
by
a fallen limb or
tree,
they
take root and turn
upwards
to reestablish a vertical orientation.
Typi-
cally
a single, downward-growing lignotuber
de-
velops
along
the side of the stem
in
contact with
the
soil,
although
in a few cases more than one had
formed
along a single
stem. On such layered
branches,
the
original
connection
to its
parent
trunk
typically
withers
away,
leaving
only
the bowed
shape
of the stem and the off-center
lignotuber
as
evidence of it
origin
from a branch
(Fig.
7).
As is the case with
lignotubers
derived from ax-
illary
buds at the
cotyledonary
node,
those
formed
by layered
branches
possess
the
ability
to
generate
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1998] DEL TREDICI:
SEQUOIA
LIGNOTUBERS 257
Figs.
1-5. 1-3. Transverse
sections of the
cotyledonary
node
region
of
15-
to
133-day-old seedlings
of
Sequoia
sempervirens.
(1)
A
15-day-old seedling showing
the
relationship
of the
superficial
meristems
(arrows)
to the
cotyledons
(c).
Bar
= 0.1
mm.
(2)
A
59-day-old
seedling showing fully
developed cotyledonary
meristems
(arrows),
foliar
pri-
mordia,
and the vascular
connection to the stele.
Bar
= 0.1 mm.
(3)
A 133-day-old seedling showing fully developed
cotyledonary
bud
(bottom)
and
two
accessory
collateral buds
(top).
Bar
= 0.3
mm. Fig. 4. A three to
four-year-old
Sequoia seedling,
collected
from
the
wild,
showing sprouting
cotyledonay
buds,
accessory
collateral
buds,
and the
remnants of a
cotyledon
(c).
Bar
= 1.0 mm. Fig. 5. A
five-year-old
greenhouse grown
seedling showing
the
proliferation
of
suppressed
buds
(arrow)
at and
above the
cotyledonay
node.
Bar =1.0 cm.
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258 MADROÑO [Vol.
45
Figs. 6-9. 6. A
large Sequoia growing along
a stream bank in the Humboldt Redwoods
State
Park
showing
extensive
root
and trunk
development
from its
exposed, downward-growing lignotuber.
Photo
by
R.
Becking.
Fig. 7. A
layered
lateral branch
of
Sequoia.
Note that the
downward-growing
induced
lignotuber
has
produced
both roots and a
vegetative
shoot. Bar
= 1.0 cm.
Fig.
8.
An
ancient
Sequoia
in
Big
Basin Redwoods
State
Park
showing
massive burl
development.
Fig.
9.
A
forest
of
Sequoias
in
Korbel, California,
resprouting
from their
lignotubers
three
years
after
clear-cutting.
both shoot
buds and roots. How
long
it
takes for
a
branch
to
develop
a visible
lignotuber
after it has
been
pinned
to the
ground
is
unknown,
but is
prob-
ably
at
least two
years.
Induced
lignotuber development
on the trunk
of
mature
trees.
Large, lignotuber-like
structures often
develop
on the lower
portions
of
the
trunk of
ma-
ture redwood trees in
response
to traumatic
injury
from
fire, wind,
or floods.
Typically
lignotubers
are
initiated above the
point
of
injury,
eventually
grow-
ing
down over
the wound to cover it.
On
very
old
trees,
extensive
growths
of
contorted callus
tissue
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1998] DEL
TREDICI:
SEQUOIA
LIGNOTUBERS 259
can
project
out from the trunk
50 cm
or
more
(Fig.
8). If
these burls come in
contact with the
ground,
which
they
often
do,
they
will
develop
both
roots
and shoots. When cut off and
placed upside
down
in a dish
of water in a warm
greenhouse,
they
will
produce
numerous
leafy
shoots within two
weeks,
and roots after six
months to one
year.
Observations
suggest
that burls on the
trunks
of
old redwood trees
originate
as wound-induced cal-
lus tissue
which,
as it proliferates,
incorporates
nearby
shoot buds into its
structure.
There
appear
to be two distinct
types
of
lignotubers
on
Sequoia,
the contorted
type,
located
mainly
on
the
lower
por-
tions of the
trunk,
which is irregular
in shape,
downward-growing
in orientation,
and covered
with
sprouts
and/or
shoot buds. The
second
type,
which occurs
higher
on the
trunk,
is nearly
hemi-
spherical
in
shape,
lacks the downward
orientation,
and
produces
comparatively
few
sprouts
or shoot
buds.
Trunk-burls are
probably
best
interpreted
as a
case of
uncontrolled
bud and cortex
proliferation
induced
by
old age,
traumatic
injury,
or environ-
mental stress.
They
serve as sites for the
production
of new shoots and adventitious roots on trees that
have been
partially
buried with silt from
flooding
or on
leaning
trees whose trunks have come into
contact with the
soil.
Discussion
According
to Strauss and
Ledig
(1985): "Archi-
tectural
patterns
established
during
the first few
months of
life
are indicative of
development
de-
cades to centuries
later,
when the
plant
has in-
creased a millionfold
in
size." The
lignotuber
of
5.
sempervirens,
which can be
fully
functional
in
four-
month-old
seedlings
and remain functional on trees
that are at least 1100
years
old,
clearly
illustrates
the truth of this observation.
Regardless
of the
age
or size of the
tree,
the redwood
lignotubers
often
resprout
within
two to three weeks of logging.
While most of these
sprouts
do
not
survive
to ma-
turity,
enough
of them do to
effectively
regenerate
a new forest
(Olson
et al. 1990).
One study
done
with
an old-growth
forest
that
had
been
clear-cut
showed that the
ability
of redwoods to resprout
(i.e.,
the number
of
sprouts
per
meter circumfer-
ence)
is
greatest
in trees that were between 200
and
400 years
of
age,
and decreases
rapidly
thereafter.
Trees more
than one thousand
years
old are able
to
resprout
at
only
20
to 25% of the
peak
rate
(Powers
and Wiant
1970).
The authors also reported
that
92% of all surviving sprouts
grow
out from the
lignotuber,
6% from the bole
proper,
and
2% from
the cut surface
of the
stump.
When a tree was
growing
on a slope
greater
than
20%,
the
sprouts
are more numerous
on the
downhill side of the
trunk.
The remarkable
ability
of redwood
trees to re-
sprout
from its basal
lignotuber, regardless
of
age,
is clearly
the basis of the
redwood's
persistence
in
the face of extensive
clear-cutting
(Fig. 9).
Throughout
its natural
range, logging
has served
to
transform
S. sempervirens
into
a clonally
reproduc-
ing species
that
spreads by means of its under-
ground
lignotuber.
Jepson
(1910)
described one col-
ony
of
45 large
redwoods that formed a third-gen-
eration
"fairy ring,"
17 m
by
15 m
across. As
sig-
nificant as lignotuber
sprouting
is for
mature
trees,
however,
the
process
is
probably
of
greater
impor-
tance to
seedlings
and
saplings
that are
struggling
to survive in dense
shade or on exposed slopes
(Becking
1968;
Canadell and Zedier
1994).
Despite
the
abundant documentation on
the im-
portance
of
Sequoia
lignotuber
sprouting
to forest-
ry,
there is very
little information available on
its
significance
in
the absence of
logging-related
dis-
turbance.
One
study
on an uncut
Sequoia
forest in
Humboldt
County
found that basal
sprouting
in red-
wood was
closely
associated with the occurrence of
fire
(Stuart 1987).
By correlating
fire scars on the
primary
trunk of the tree
with basal
sprouts
from
its
lignotuber,
the author determined that
during
the
"pre-settlement period"
(between
1775
and
1875)
fires
occurred
regularly
in
the
forest,
at an
average
interval of
24.6 ±2.8 years.
Other
studies,
which
analyzed
fire
scars on the cut
stumps
of
old-growth
redwoods,
support
the idea that fires were
common
in the redwood
region
prior
to
European
settlement
(Fritz
1931;
Jacobs et
al. 1985;
Finney
and Martin
1992).
These
findings
are consistent with studies
in
other Mediterranean
climates which
report
the oc-
currence of lignotuber-producing angiosperms
in
habitats where
fire,
or other
types
of
recurring
dis-
turbance,
is common
(James
1984;
Mesleard and
Lepart
1989).
The trunk of a redwood
tree,
above
the
lignotu-
ber,
also shows a strong ability
to
resprout
follow-
ing
traumatic
injury.
In the older
forestry
literature,
there are numerous
reports
of
large
trees,
entirely
defoliated
by
fire,
that
sprout vigorously
to form
lush "fire columns"
(Jepson
1910; Fritz
1931).
Similarly,
the author
has observed
recently
blown
down trees that
sprouted
new
growth along
the en-
tire
length
of
the
horizontal trunk. Fink
(1984)
stud-
ied the
ability
of
Sequoia
stems
to
resprout
follow-
ing
injury
and found that clusters of
replacement
buds
developed exogenously
in
the needle axils
of
young
branches over a one to two
year
period.
Ex-
cept
for the
length
of time
involved,
the
process
he
described for the development
of preventitious
shoot buds is
very
similar
to
that of
the
cotyledon-
ary
buds described
in
this
paper.
One
must
keep
in
mind, however,
that the
lignotuber
formed
at
the
cotyledonary
node is under strict
genetic
control
while those that
develop
elsewhere
on the trunk are
under environmental
control. In this
regard,
Se-
quoia is similar to
Ginkgo
biloba which
produces
positively geotropic
lignotubers
from
axillary
cot-
yledonary
buds
(basal
chichi),
as well as induced
lignotubers
(aerial chichi)
on its trunk and branches
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260 MADROÑO [Vol.
45
(Del Tredici
1992,
1997).
As is the case with Se-
quoia,
shoot and
root
regeneration
by
the
Ginkgo
biloba
lignotuber play
an
important
role in the
per-
sistence
of the
species
in its native
habitat in
the
temperate
forests
of eastern
China
(Del Tredici et
al. 1992).
From
both
the
morphological
and
physiological
perspectives,
lignotuber-generated
shoots can be
considered
"juvenile"
relative
to
the rest of the
tree
(Greenwood
1995).
This
conclusion is
supported
by
in vitro
studies which
found
that tissue cultures
started
with
lignotuber
shoots
from the
base of a
90-year-old
Sequoia
were more
vigorous
and
rooted
more
readily
than those
started with shoots
from
the crown
of the same
tree
(Bon
et
al. 1994).
The
authors
also identified
numerous
membrane-asso-
ciated
proteins
that were
synthesized
in greater
abundance
in cultures
derived from
lignotuber
shoots
that
those derived
from the
upper portions
of the tree.
Certainly
it is not
by
chance
that Se-
quoia
was the first
conifer to be successfully
cul-
tured
using
in vitro
techniques,
and that
the cultures
were
derived from
lignotuber
sprouts
(Ball 1950).
Acknowledgments
I
would like to
express
my
thanks
to: Dr. Rudolf Beck-
ing
of
Areata, California,
who
freely
shared his extensive
knowledge
of
the redwood
forest with
the
author;
Sheila
Morris of
Vancouver,
British
Columbia,
who
provided
technical
support
with
the
staining
and
sectioning
of the
seedling
material;
and
Dr. Paul
Groff,
whose
work first
stimulated
my
ideas on
the
subject
of
Sequoia
lignotubers.
I would
also like
to thank the
Highsted
Foundation of
Redding,
Connecticut,
for
financial
support;
the
green-
house staff
of the Arnold
Arboretum,
for
growing
the
plants
used
in this
study;
and the
Organismal
and Evolu-
tionary Biology Department
of Harvard
University
for al-
lowing
me to use
their
microscopes.
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