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Summary Reiteration is the process whereby architectural
units are replicated within a tree. Both immediate (from apical
buds) and delayed (from suppressed or adventitious buds) reit
-
eration can be seen in many tree species where architectural
units ranging from clusters of shoots to entire branches and
stems are replicated.In large old trees and suppressed trees, de
-
layed reiteration occurs without an obvious external stimulus
such as defoliation or traumatic loss of the branch apex. This
suggests that, in trees that are growth-limited, reiteration is an
adaptive mechanism for crown maintenance. We discuss theo-
ries about the aging process and how delayed adaptive reitera-
tion may help maintain crown productivity and increase lon-
gevity. These include: (1) reducing the respiration/photosyn-
thesis ratio; (2) increasing hydraulic conductance to newly de-
veloping foliage; (3) reducing nutrient loss from the tree; and
(4) rejuvenating the apical meristem. The ability to reiterate
various architectural units may contribute to increasing life
-
time reproductive output by prolonging tree longevity. Further
studies on the physiological and ecological implications of re
-
iteration are needed to understand its adaptive significance in
the life history of trees.
Keywords: cellular senescence, crown productivity, hydraulic
architecture, longevity, nutrient limitation.
Introduction
Reiteration is the process whereby architectural units are repli
-
cated within a tree (Hallé et al. 1978). There are two basic
types of reiteration: immediate or sylleptic reiteration (nomen
-
clature after Bégin and Filion 1999), which occurs from se
-
quential growth of an apical bud, and delayed or proleptic reit
-
eration, which occurs from suppressed or adventitious buds.
Reiteration often occurs in response to some trauma such as
defoliation or damage to the apical bud (Bryan and Lanner
1981, Del Tredici 2001) or pruning. Delayed reiteration in the
form of epicormic sprouting is well documented in many spe
-
cies of angiosperms (Wignall et al. 1987, Bellingham 2000,
Del Tredici 2001). In silviculture, the occurrence of delayed
reiteration from the main stem (epicormic branching) has neg
-
ative implications because it causes unwanted knots in the
wood (Cosens 1952, Stone 1953). Epicormic branching has
been observed to occur after stand thinning (Jemison and
Schumacher 1948, Wignall and Browning 1988a) and may be
a response to damage or increased light availability (Jemison
and Schumacher 1948, Berntsen 1961, Blum 1963, Batzer
1973, Hibbs et al. 1989).
In many species, however, both immediate and delayed reit-
eration occur without any apparent trauma as part of the nor-
mal development of the tree and, hence, this process is referred
to as adaptive reiteration (Bégin and Filion 1999). In young
Picea mariana (Mill.) BSP, delayed adaptive reiteration pro-
duces several “generations of replicas” of architectural units
within the crown “as part of the normal development of the
tree” (Bégin and Filion 1999). In Fraxinus pennsylvanica var.
subintegerrima (Vahl) Fern. and Thuja occidentalis L., basal
reiteration (delayed reiteration on proximal branch axes)
maintains leaf area in the inner crown (Remphrey and
Davidson 1992, Briand et al. 1992). In Larix occidentalis Nutt.
and Pseudotsuga menziesii var. glauca (Beissn.) Franco,
epicormic branching occurs routinely unrelated to any appar
-
ent injury to intact branches (Bryan and Lanner 1981, Lanner
1996).
Delayed adaptive reiteration is of particular interest because
it is proposed as a mechanism of growth that maintains crown
productivity and prolongs tree longevity (Bryan and Lanner
1981, Lanner 1996, Lanner 2002, Ishii and Ford 2002). In
450-year-old Pseudotsuga menziesii (Mirb.) Franco trees, epi
-
cormic buds are released from suppression in the absence of
any apparent trauma to the branch apex, and grow to form ar
-
chitectural units (shoot cluster units) consisting of 20–300 fo
-
liated shoots (Ishii 2000, Figure 1a). The maximum observed
age of shoot cluster units is 24 years, suggesting that continual
production, growth and death results in the turnover of shoot
cluster units. As a result, the branch is maintained as a stable
population of shoot cluster units (Figure 1b). In old
P. menziesii trees, delayed reiteration occurs regularly from
older branch axes (basal reiteration, Ishii et al. 2002), as well
as from the main stem (epicormic branching, Ishii and Wilson
2001). In the former case, reiterated foliated shoots may de
-
Tree Physiology 27, 455–462
© 2007 Heron Publishing—Victoria, Canada
Physiological and ecological implications of adaptive reiteration as a
mechanism for crown maintenance and longevity
HIROAKI T. ISHII,
1,2
E. DAVID FORD
3
and MAUREEN C. KENNEDY
3
1
Graduate School of Science and Technology, Kobe University, Kobe 657-8501, Japan
2
Corresponding author (hishii@alumni.washington.edu)
3
College of Forest Resources, University of Washington, Seattle, WA 98195-2100, USA
Received January 31, 2006; accepted May 18, 2006; published online December 1, 2006
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velop into large branch axes, whereas in the latter case, reiter
-
ated shoots may develop into whole branches from the trunk.
Extensive three-dimensional mapping of branches in
old-growth trees of P. menziesii, Sequoia sempervirens
(D. Don.) Endl., Seqoiadendron giganteum (Lindl.)
Buchholz., Thuja plicata Donn ex. D. Don and other species
(Ishii and Wilson 2001, Van Pelt 2001) illustrates how crowns
are created through the process of reiteration.
Immediate adaptive reiteration occurs in the shaded lower
crowns of old Thuja plicata trees, where a branch axis turns
upward and so reiterates the tree’s main stem (Edelstein and
Ford 2003, Figure 1c). The growth of the reiterated vertical
branch axis is less than that of lateral axes arising from it, so
that the entire reiterated structure resembles the architecture of
a suppressed understory tree growing on the mother tree. In
suppressed understory trees of Fagus sylvatica L., epicormic
branching contributes to maintaining foliage area (Nicolini et
al. 2001). These observations suggest that adaptive reiteration,
both immediate and delayed, occurs in trees whose growth is
limited by age, size or environmental factors, or a combination
thereof. In this paper we consider two questions: What pro
-
cesses initiate adaptive reiteration? What effects might adap
-
tive reiteration have on the growth and aging process of tree
crowns?
Possible causes of adaptive reiteration
Both immediate and delayed reiteration involve some disrup
-
tion to the normal pattern of architectural development (Hallé
et al. 1978). Young trees show hierarchical architecture, where
456 ISHII, FORD AND KENNEDY
TREE PHYSIOLOGY VOLUME 27, 2007
Figure 1. Examples of adaptive reiteration. (a) Epicormic shoots develop on a branch axis proximal to an actively growing
branch apex (delayed reiteration) in old Pseudostuga menziesii. Epicormic shoots generally develop at positions where lateral
axes on the parent branch are no longer producing current-year shoots (Ishii and Ford 2001). With increasing age, lateral axes
on the parent branch elongate and grow downward, whereas newly produced epicormic shoots grow horizontally above the
parent axis. (b) Two mid-crown branches of P. menziesii viewed from above. The entire lengths of the branches are covered
with foliage. New shoots are produced not only at the tip of the branch, but by epicormic sprouting at proximal positions (E1,
E2 and E3, where 1 indicates the most recently produced shoot). Arrows indicate direction of main branch axis. (c) Immediate
reiteration in the shaded lower crown of old Thuja plicata. A lateral branch from the main stem of the tree with an initially hori
-
zontal, plagiotropic axis (indicated by dotted white line) turns upward to reiterate a vertical, orthotropic axis. The growth of the
vertical axis is less than that of lateral axes arising from it and the entire reiterated structure resembles a suppressed understory
tree attached to the parent tree. (d) With increasing age, the frond-like foliage on the lateral axes begins to elongate and grow
downward. Epicormic shoots are produced from their junction with the lateral axis (delayed reiteration) and eventually
supercede the older fronds.
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increasingly small architectural units, from the main stem to
branches and shoots, are sequentially connected, whereas old
trees show polyarchical architecture with repeated reiterations
resulting in smaller architectural units arising from much
larger ones (Barthélémy et al. 1989, Millet et al. 1998, Millet
et al. 1999). During the course of normal architectural devel
-
opment, hierarchy among architectural units is maintained by
apical control where dominant axes restrict growth of subordi
-
nate axes proximal to them (Wilson 2000). In addition, apical
dominance prevents suppressed buds from growing out (Cline
and Sadeski 2002). However, in large old trees and suppressed
trees, decreasing growth rate and vigor of apices may result in
loss of apical control as well as loss of apical dominance
(Moorby and Wareing 1963, Barthélémy et al. 1989). Loss of
apical control may cause subordinate axes to grow like domi
-
nant apical axes (immediate reiteration) and loss of apical
dominance may cause suppressed buds to be released from
dormancy (delayed reiteration).
There is no well-established theory explaining how delayed
adaptive reiteration is initiated. Experiments on angiosperms
show that suppressed buds can be released following decapita
-
tion of the shoot apex. Application of auxin in place of the re
-
moved shoot apex prevents release of suppressed buds (Bow-
ersox and Ward 1968, Bachelard 1969, Vogt and Cox 1970,
Wignall and Browning 1988b) and girdling the phloem can ne-
gate the effect of the applied auxin. Achieving these effects de-
pends on the timing and location of the girdle (Cline 2000),
and on the removal of major lateral buds just below the apex.
Experimentally applied indoleacetic acid (IAA) prevents bud
release but the concentration of endogenous IAA in cambial
regions actually increases in spring when the buds grow—in-
dicating that natural bud release is not the result of a decrease
in endogenous IAA concentration (Wignall and Browning
1988b). This suggests that the buds themselves may generate
or mobilize the stimulus and the resources needed to escape
IAA inhibition. Bachelard (1969) made a series of experi
-
ments over a year with explants of +50-year-old Eucalyptus
polyanthemos Schauer where growth substances and sucrose
were applied after decapitation and temperature and light were
varied. He suggests there is “… a competitive relationship be
-
tween cambial activity and epicormic shoot production” and
“epicormic shoot production is favored at times when the cam
-
bium is dormant rather than it being simply a response to re
-
moval of IAA inhibition.”
Epicormic shoots are found on trees of all ages. For exam
-
ple, considerable production of small epicormic shoots occurs
in young (~30-year-old) trees of P. menziesii (Hollatz 2002).
However, these epicormic shoots do not persist, typically dy
-
ing before their third year. Similar types of short-lived
epicormic shoots are found on young Picea sitchensis
(Bongard) Carriere, Picea rubens Sarg. and Abies grandis
(Dougl. Ex D.Don) Lindl (E.D. Ford and M.C. Kennedy,
unpublished). Field observations report epicormic shoot
growth as a characteristic of stems of suppressed trees under
-
going slow growth (Fontaine et al. 1999, Quercus petrea
Mattusch. Liebl.; Nicolini et al. 2001, F. sylvatica; and
Nicolini et al. 2003, Dicorynia guianensis Amshoff). Nicolini
et al. (2001) measured distinct sequences of epicormic shoot
development in suppressed trees of 36- to 120-year-old F.
sylvatica that were gradually covered in epicormic branches
from the stem base to the crown. Formation of this new crown
of epicormic branches was combined with a sharp reduction in
stem cambial activity (partial rings, if any) but then girth incre
-
ment resumed following the establishment of epicormic
branches. Nicolini et al. (2003) observed that epicormic
branching in D. guianensis is related to both low primary and
secondary growth of the parent axis. They propose that the de
-
gree of epicormic branching may be used as an indicator of
tree age and vigor.
Physiological implications of delayed adaptive reiteration
As a working hypothesis, we might consider that delayed
adaptive reiteration occurs on branches and stems where dor
-
mant buds are present and apical and cambial growth have
slowed—but how might this contribute to maintaining crown
productivity? There are several theories on why tree growth
declines with age. These can be classified as associated with:
(1) increasing respiration/photosynthesis ratio; (2) hydraulic
limitation; (3) nutrient limitation; and (4) genetically pro-
grammed senescence (Ryan and Yoder 1997). How could de-
layed reiteration mitigate effects of these limitations on
growth?
Before considering each theory individually, it is important
to consider delayed adaptive reiteration in the context of
branch growth, decline and death. A useful starting point is the
theory of branch autonomy, which proposes that “no branch
imports carbohydrate from its parent tree after its first year”
and that “each branch satisfies its own material and energy re-
quirements before exporting carbohydrate to the rest of the
tree, then when light is the primary limiting factor, the critical
characteristics of a branch’s carbohydrate economy … are
largely independent of the tree to which it is attached”
(Sprugel 2002). A branch should die when it cannot satisfy its
own demand for carbon. Sprugel (2002) presents data from his
own investigations contradicting the branch autonomy theory
and reviews other research on young trees showing that
branches on suppressed trees are able to grow and produce
new foliage at solar irradiances under which branches on dom
-
inant trees die. He also reviews work showing that stresses
other than shading have the same effect: “a stressed branch on
a stressed tree does better than a similarly stressed branch on a
tree where some branches are relatively unstressed,” a process
known as correlative inhibition (Stoll and Schmid 1998, Take
-
naka 2000).
Our observations in large old trees suggest further contra
-
diction to the branch autonomy theory. In an old-growth conif
-
erous forest in western Washington, branch extension growth
of short trees is greater in the upper crown than in the lower
crown, corresponding to the vertical gradient in light availabil
-
ity (Figure 2). In trees taller than 40 m, however, extension
growth of branch tips is suppressed in all parts of the crown,
suggesting that branch growth is determined by factors other
than the light environment. Delayed adaptive reiteration is a
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ADAPTIVE REITERATION: A MECHANISM FOR CROWN MAINTENANCE 457
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characteristic of old trees that also appears to contradict the
branch autonomy theory. A whole branch does not die, but fo-
liated sections on it are superceded by the development of
more proximal ones that themselves extend and then may be-
come superceded by the same sequence. Proximally produced
reiterated sections are able to out-compete more distal ones for
growth resources and this maintains branch productivity. We
propose that delayed adaptive reiteration is a dynamic process
that maintains growth under generally stressful conditions.
Increasing respiration/photosynthesis ratio
Yoda et al. (1965) observed that the proportion of non-produc
-
tive tissue relative to productive tissue increases with increas
-
ing tree size. Based on this observation, it was proposed that
increasing respiratory demand may lead to growth decline
with increasing tree size (Westing 1964, Zimmermann and
Brown 1971, Clark 1983, Remphrey and Davidson 1992).
Gerrish (1990) found that the volume of respiring tissue (sap
-
wood and inner bark) relative to leaf mass was greater in ma
-
ture trees than in juvenile trees of Metrosideros polymorpha
Gaud., and proposed that death of shaded branches followed
by epicormic branching would contribute to maintaining
crown productivity by reducing the amount of respiratory tis
-
sue. However, later studies have shown that maintenance res
-
piration represents only a small percentage of the total carbon
budget (Ryan et al. 1995) and remains relatively constant at
the stand level after canopy closure (Ryan and Waring 1992).
These findings suggest that increases in respiratory demand
may not explain the decline in productivity with increasing age
(Gower et al. 1996). Nevertheless, death of large sections of
branches and their replacement through delayed reiteration re
-
sults in a significant reduction of non-productive tissue and
may contribute to reducing maintenance respiration
(Remphrey and Davidson 1992).
Ryan and Waring (1992) suggested that the decline in pho
-
tosynthesis with increasing age may be a more plausible expla
-
nation for declining growth. Lower maximum photosynthesis
rates (A
max
) have been observed in old trees than in young trees
(Yoder et al. 1994) and saplings (Thomas and Winner 2002).
In old trees of both P. menziesii and T. plicata, epicormic
shoots produced by delayed reiteration grow over the top of
the parent branch axis (Figures 1a and 1d). Typically, older lat
-
eral axes on the parent branch begin to grow downward as they
elongate, whereas newly produced epicormic shoots grow hor
-
izontally above the parent axis. Our measurements indicate
that shoots on reiterated axes receive more light than shoots on
lateral axes of the parent (E.D. Ford, unpublished data). In ad
-
dition, epicormic shoot production occurs more frequently at
outer-crown positions along the branch where light conditions
are favorable for new shoot production (Ishii et al. 2002). De
-
layed adaptive reiteration, by placing new shoots in better illu-
minated areas of the crown, may result in greater A
max
of new
shoots compared with older shoots that are less well illumi-
nated, and in higher daily photosynthetic production (A
Day
,
Schoettle and Smith 1998).
Hydraulic limitation
As trees grow larger, hydraulic conductance decreases as a re-
sult of the increasing length and decreasing conductivity of xy-
lem tissue (Tyree and Ewers 1991, Ryan and Yoder 1997,
Mencuccini 2002, Phillips et al. 2002). This may limit tree
growth by imposing limitations on stomatal conductance and
photosynthesis (hydraulic limitation hypothesis, Ryan and
Yoder 1997, Ryan et al. 2006). There may be some homeo
-
static mechanisms that partially compensate for reduced hy
-
draulic conductance with increasing tree size, such as a reduc
-
tion in leaf area/sapwood area ratio (McDowell et al. 2002),
increased reliance on stored water (Phillips et al. 2002) and in
-
creased reliance on hydraulically redistributed water (Brooks
et al 2003); however, these compensatory processes may come
at an increased carbon cost. Carbon allocation to transport tis
-
sue increases and allocation to leaf area decreases with in
-
creasing tree age, and this may contribute to decreasing pro
-
ductivity (Magnani et al. 2000). Thus, allocation to transport
tissue needed to maintain a constant water transport capacity
increases with increasing plant height (Mencuccini 2003). In
addition, the number of annual nodes and junctions, which
form constrictions along the hydraulic pathway and reduce hy
-
draulic conductance (Larson and Isebrands 1978, Rust and
Hüttl 1999), increases with increasing branch age, and hydrau
-
lic conductivity of branch axes decreases with increasing dis
-
tance from the trunk (Ewers and Zimmermann 1984a, 1984b).
Reiteration may counter these trends.
Both epicormic branching and basal reiteration significantly
shorten hydraulic path lengths to new foliage. In addition, the
458 ISHII, FORD AND KENNEDY
TREE PHYSIOLOGY VOLUME 27, 2007
Figure 2. Branch extension growth of four conifer species in the
old-growth forest at the Wind River Canopy Crane Research Facility,
WA. The crown of each tree was divided into three equal layers (up
-
per, middle and lower) and branches were sampled near the mid-
height of each layer. Branch extension growth is the mean length of
annual increments at the branch tip from 1998 to 2001.
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reiterated axes are directly connected to lower-order axes such
as the main stem and large branch axes, which have high hy
-
draulic conductivity (Tyree and Ewers 1991, Kozlowski and
Pallardy 1996). Thus, delayed reiteration alters hydraulic ar
-
chitecture and reduces the length and complexity of the hy
-
draulic pathway. In the crown of Quercus acutissima Carruth.,
soil-to-leaf hydraulic conductance was higher for epicormic
sprouts than for branch terminal shoots, suggesting that
greater hydraulic conductance may contribute to the vigorous
growth of sprouts in this species (Ito 1996). In old P. menziesii
trees, carbon isotope ratios (δ
13
C) were lower in current-year
needles on epicormic shoots than in current-year needles on
distal shoots of the parent branch, indicating lower time-aver
-
aged photosynthetic water-use efficiency (carbon gain per wa
-
ter transpired), i.e., less water stress for epicormic shoots (Fig
-
ure 3). These observations suggest that delayed reiteration, by
producing new shoots at more proximal positions and on
lower-order axes, increases hydraulic conductance to new fo
-
liage, thus mitigating hydraulic limitation on tree growth.
Nutrient limitation
As trees grow larger, absorbed nutrients are sequestered in the
plant body. Although the nutrient content of woody organs is
low, woody organs are slow to decompose. As the forest ages
an increasing quantity of nutrients is sequestered in wood that
may result in decreasing nutrient availability with increasing
tree age and impose limitations on tree growth (the nutrient
limitation hypothesis, Gower et al. 1996). Where plant growth
is nutrient limited, nutrient loss can be reduced by increasing
the life-span and decreasing the nutrient content of plant tis
-
sue, and by nutrient resorption from senescing tissue (Aerts
1995). In seedlings of Quercus pagoda Raf., epicormic sprouts
induced by clipping are strong sinks for carbon allocation
(Lockhart et al. 2003). Epicormic sprouts produced by de
-
layed adaptive reiteration may be strong sinks for trans
-
location of carbon and nutrients from senescing parts of the
tree. This could reduce nutrient loss and mitigate nutrient
limitation by conserving nutrient pools within the tree body.
Genetically programmed senescence
As trees grow, a genetically programmed aging process may
lead to decreased growth potential of meristems, known as the
maturation, or senescence, hypothesis. In Picea rubens Sarg.,
differences in foliar morphology between scions from mature
and old trees persisted for three growing seasons after grafting
to a common rootstock, suggesting that shoots from old trees
have inherently lower growth potentials (Day et al. 2001).
This may be the consequence of programmed changes in gene
expression that lead to cellular senescence (Bender 2004).
These molecular changes, however, may not be irreversible.
Studies of methylation of carbon residues in genomic DNA in
needles of young and mature Pinus radiata, and in the rejuve-
nation process of propagated individuals, indicate that the ex-
tent of genomic DNA methylation can serve as a marker of
both aging and reinvigoration (Fraga et al. 2002). This sug-
gests that physiological and chronological age can differ and
that molecular mechanisms can be induced that result in reju-
venation of axillary buds, possibly through DNA
demethylation.
In both angiosperms and gymnosperms, relative growth rate
and net assimilation rate do not change with age of grafted sci
-
ons, whereas significant decreases with increasing age are ob
-
served for the individual donors in the field, suggesting that in
-
creasing size and complexity with increasing age, not an in
-
trinsic aging process, contributes to the growth decline in large
old trees (Mencuccini et al. 2005). Similarly, young shoots
grafted into upper crowns of tall Cryptomeria japonica D. Don
trees show light-saturated photosynthetic rates and stomatal
conductances similar to those of intact shoots (Matsuzaki et al.
2005). Shoots at the tops of the crowns of old trees of Pinus
longaeva D.K. Bailey (up to 4712 years old) show no sign of
reduced growth when compared with shoots on young trees (>
12 years old) (Connor and Lanner 1989). In tall
S. sempervirens trees, foliage structure changes with increas
-
ing tree height such that needles became smaller over a range
in tree height from 2 to 112 m, but when a branch segment
from a 90-m-tall tree is rooted in wet soil it produces needles
of increased size (Koch et al. 2004). Because current shoots on
an existing tree are produced by meristems of the same chro
-
nological age, this suggests that factors associated with height,
not meristem age, determine needle morphology.
In the crowns of 450-year-old P. menziesii trees, original
non-epicormic branches in the middle crown have an average
of 148 annual rings, whereas epicormic branches in the lower
crown have only 94 annual rings on average (Ishii et al. 2002).
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ADAPTIVE REITERATION: A MECHANISM FOR CROWN MAINTENANCE 459
Figure 3. Carbon isotope ratios (δ
13
C, ‰) of current-year needles on
epicormic shoots (䊊) and on shoots at the distal end of the parent
branch (䊉) in 450-year-old Pseudotsuga menziesii trees. Where pos
-
sible, pairs of shoots (epicormic and parent) were sampled from the
same branch. Sample branches were chosen from the lower crown to
minimize differences in light environment between shoots (paired t
test of canopy openness: t = 0.786, P = 0.447). (a) Epicormic shoots
are closer to the trunk than parent shoots and δ
13
C values of cur
-
rent-year needles on epicormic shoots were significantly lower than
those of current-year needles on the parent (paired t test, t = 3.610, P =
0.003), indicating lower time-averaged water-use efficiency (carbon
gain per water transpired), i.e., less water stress for epicormic shoots.
(b) δ
13
C values decreased with increasing height. Similar height-re
-
lated changes in δ
13
C were found by Winner et al. (2004). A linear
mixed effects model (lme, R statistical software) with random slopes
grouped by branch indicated that δ
13
C values increased with increas
-
ing branch height and were lower for epicormic shoots than for parent
shoots (P < 0.05).
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In addition, basal reiteration occurs from branch axes as old as
58 years. Suppressed buds grow just enough to keep up with
the expanding cambium (Kozlowski 1971) and, thus, meri
-
stems produced by epicormic sprouting have undergone less
cell division than sequentially growing meristems. Although
the chronological age of epicormic and sequential meristems
may be the same, the physiological age of meristems produced
by epicomic sprouting may be younger. Physiological charac
-
teristics and growth of meristems may be determined by a
shoot’s relative position in the tree rather than by chronologi
-
cal age of the meristem.
Reiterated shoots may out-compete older shoots for internal
resources (water and nutrients), thereby enabling them to uti
-
lize light more efficiently. Simulation studies indicate that, in
old, growth-limited branches of P. menziesii, reiteration signif
-
icantly increases branch longevity (Kennedy et al. 2004). Sim
-
ulations over 300 years, however, indicate that there are limita
-
tions to reiteration with increasing branch size and complex
-
ity: after repeated reiterations, the capacity for further reitera
-
tions decreases. This implies that, although reiteration
increases branch longevity, the process is itself subject to the
limitations that we propose it serves to overcome.
Ecological implications of adaptive reiteration
Many woody species have the ability to resprout in response to
injury. The frequency and severity of disturbances determines
allocation to resprouting relative to seed production in woody
plants (Bellingham 2000). Resprouting occurs at various spa-
tial scales depending on disturbance severity (amount of
aboveground biomass lost): sprouting of shoots from axillary
buds, basal reiteration from branches, epicormic branching
from the main stem and resprouting of stems from stumps. The
resprouting habit allows species to exploit the persistence
niche (sensu Bond and Midgley 2001) by surviving through
disturbances.
Adaptive reiteration, however, is not an injury response.
Crown maintenance by epicormic sprouting is a normal life-
history trait (Lanner 1996) that prolongs tree life span. Young
trees grow rapidly thereby exploring new space, whereas, in
old trees, reiteration realizes more efficient exploitation of
space already occupied. For old trees, traits associated with
persistence, such as long-term resistance to abiotic stresses,
maintenance of crown productivity and hydraulic conductance
and conservation of nutrients, may be more important for sur
-
vival than a high growth rate. Lower growth rates may be an
adaptive trait in old trees for optimizing resource-use effi
-
ciency and long-term survival, as well as reproductive success
(Day et al. 2002).
For long-lived species such as trees, persistence and mainte
-
nance of reproductive output would lead to greater fitness. For
example, longevity of aerial stems of Lindera umbellata
Thunb. var umbellata, a clonal shrub, conforms to the theoreti
-
cal model for maximizing lifetime reproductive output of indi
-
viduals (Fujiki and Kikuzawa 2006), suggesting that the tim
-
ing of sprouting may be an adaptive trait for maximizing indi
-
vidual fitness. Simulation studies demonstrate that delayed
adaptive reiteration significantly increases branch longevity in
old P. menziesii trees, particularly when compared with
A. grandis, which has a similar basic branching system but
with no adaptive reiteration (Kennedy et al. 2004). Increased
longevity may allow pioneer species such as P. menziesii to
maintain reproductive output between infrequent disturbance
events, thus increasing their fitness (Ishii and Ford 2002).
There are many studies on the adaptive significance of stem
and root sprouts and how natural populations of stems are
maintained by sprouting in various woody species (e.g., Tap
-
peiner et al. 1991, Sakai et al. 1995, Ishii and Takeda 1997, Ito
et al. 1999, Homma et al. 2003). Several studies have also
compared growth and physiology of stump sprouts relative to
seedlings (e.g., Kauppi et al. 1990, Kauppi 1991, Ito et al.
1995). In contrast, the physiological and ecological implica
-
tions of within-crown sprouting (delayed reiteration) have re
-
ceived less attention. We propose that adaptive reiteration
(both immediate and delayed) is a mechanism for maintaining
crown productivity and reproductive output in large old trees
that have reached maximum size and in growth-limited sup
-
pressed trees.
Further studies are needed to elucidate the physiological
mechanisms and conditions under which adaptive reiteration
occurs. A species’ ability to reiterate architectural units within
the crown may be associated with the capacity to produce dor-
mant buds. Dormant buds form a bud bank that contributes to
reiteration of architectural units within the tree, and is analo-
gous to the seed bank that contributes to regeneration of indi-
viduals on the forest floor. As with the seed bank, species
adapted to frequent disturbances may maintain a large bud
bank. Species adapted to infrequent disturbances may main-
tain a relatively small bud bank, but sprouting may occur regu
-
larly (adaptive reiteration) as a mechanism of crown mainte
-
nance. Comparative studies on different species’ capacity for
reiteration may elucidate the adaptive significance of this
process in the life history of trees.
Acknowledgments
We thank B.J. Bond, R.M. Lanner, M. Mencuccini and S. Ito for stim
-
ulating discussion and ideas that led to the development of this paper,
and R.H. Waring for funding the δ
13
C measurements on Douglas-fir
branches. We are grateful to Tom Hinckley and Steffan Rust for help
-
ful criticism. We also thank F.C. Meinzer and G. Goldstein for invit
-
ing HTI to present at the symposium at the 4th International Canopy
Conference and for coordinating this collection of papers.
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