Opinion

Limits to Tree Growth and Longevity

Sergi Munné-Bosch1,*

Tree growth and longevity are key features to understand fundamental issues of Highlights
plant biology, environmental sciences, and current forest management plans. Long-lived trees with extreme longev-
ity maintain some growth capacity and
Here I discuss current evidence on the limits of tree growth and longevity and
defy aging.
present a new conceptual framework to understand how and why they are
closely interconnected. Despite the tremendous plasticity of trees, growth and Mosaic-like organization of meriste-
matic (growing) points is one of the
longevity are limited not only by biotic and abiotic stresses, but also by most important mechanisms behind
age-related structural constraints such as height-related hydraulic limitations their extreme longevity.
and vascular discontinuities, which are strongly species specific. Continuous
Senescence cannot be gauged in
growth and plastic branching may serve as a means to reach extreme longev- long-lived trees growing in their natural
ities in some nonclonal trees, but even in these millennial organisms immortality habitat because of limited sample size
at advances ages.
can be attained only through the germ line.
Despite cases of extreme longevity in
The Importance of Tree Growth and Longevity nonclonal trees, immortality can be
Tree growth and longevity are fundamental processes in our current understanding of plant biology achieved only through clonal repro-
duction or the germ line.
and environmental sciences. Trees are unique in terms of development, stress (see Glossary),
resilience, and longevity. Some trees not only typically survive for several hundreds of years but can
even live for millennia, making our maximum lifespan quite insignificant in comparative terms. The
longest-lived nonclonal living gymnosperm tree individual known to date, a specimen of bristlecone
pine (Pinus longaeva) in the White Mountains in California, is 5067 years old [1]. Nonclonal angio-
sperm trees can also attain extraordinary longevity, such as the baobabs growing in Africa, some
individuals attaining ages well above 2000 years [2]. Although dendrochronology and radiocarbon
dating had not developed as a science, long-lived trees appeared in Renaissance paintings related to
aging, mortality, and death (Box 1 and Outstanding Questions).

More recently, studies of tree meristems have pointed to clues to understanding why long-lived
trees may not suffer the wear and tear of aging [4]. The mosaic-like disposition of growing
meristematic points within the canopy seems to prevent large mutations from occurring over time
[5,6]. Furthermore, slow mutational rate in these meristems explains, at least in part, the mecha-
nisms behind the extreme longevities seen in some long-lived trees [7,8]. A better understanding of
the mechanisms behind extreme longevities has tremendous implications not only for basic but
also for applied science. Tree growth and longevity are essential players governing the diversity
and productivity of the planet’s forests [9,10] and better knowledge of the factors controlling them
is essential to improve forest management [10,11]. Interestingly, some long-lived trees not only are
unique in terms of longevity on Earth [1], but retain the capacity for continuous growth over
hundreds of years or even millennia [12–14] and clearly pose a threat to the idea that immortality is
impossible (as reviewed previously [15–17]). Here I discuss novel evidence for, as well as against, 1
Department of Evolutionary Biology,
constraints on tree growth and longevity. Furthermore, I present a new conceptual framework for a Ecology and Environmental Sciences,
University of Barcelona, Faculty of
better understanding of the relationship between tree growth and longevity.
Biology, Av. Diagonal 643, E-08028
Barcelona, Spain

Limits to Tree Growth

A number of abiotic and biotic stress factors, acting alone or in combination, limit growth in *Correspondence:
plants [18]. Trees are obviously no exception to this limitation [19]. Indeed, the definition of smunne@ub.edu (S. Munné-Bosch).

Trends in Plant Science, November 2018, Vol. 23, No. 11 https://doi.org/10.1016/j.tplants.2018.08.001 985
© 2018 Elsevier Ltd. All rights reserved.
stress is intrinsically associated with growth. Among a number of stress factors, drought is one Glossary
of the most important, since it limits growth through its direct effects on cell turgor, a Aging: measure of time (without
prerequisite for cell growth [20]. In a study of the height gradients of functional leaf character- implicitly negative connotations).
istics in redwoods (Sequoia sempervirens), the tallest known trees on Earth (112.7 m), tree Apical dominance: the
phenomenon whereby the growth of
height appeared to be limited to 130 m [18]. In that study, it was shown that as trees grow taller, the main, central stem of the plant is
increasing leaf water stress due to hydraulic and mechanical constraints may ultimately limit leaf dominant over other, side stems.
expansion and photosynthesis, thereby preventing further height growth even with ample soil Canopy: aboveground plant parts.
Dendrochronology: tree-core
moisture ([21]; see also [22] for details of hydraulic and mechanical constraints). Interestingly,
dating to estimate age, growth, and
the mass-per-area ratio of leaves found at a height of 112 m was 6.5 times greater than at 50 m. past climate.
This, and the fact that net photosynthesis rates in the tallest parts of the tree are close to zero, Half-life: time over which half of the
indicate severe stress [21]. Increased height forces new iterated shoots to live under conditions individuals can be expected to die.
Iteration: new lateral growth point in
of extreme stress. In other words, height alone limits the vertical growth of trees, because of the
the canopy derived from the
limits imposed by such severe stress. Besides the hydraulic and mechanical constraints differentiation of an axillary meristem.
associated with height, it should be borne in mind that new shoots formed at heights above Life expectancy: measure of the
100 m in these trees will compete for nutrients and photoassimilates with the other shoots that average time an organism is
expected to live.
already exist [23]. Nutrient uptake will be limited by hydraulic constraints, but photoassimilates
Lifespan: duration of life.
will be limited by the source–sink relationships established between old and new shoots [24]; Maximum lifespan: maximum
this aspect is not only important for modeling forest growth [25] but also essential to understand duration of life for a given species.
production in fruit trees [26]. Meristem: undifferentiated plant
stem cell that potentially forms a new
organ.
The height, size, and age of trees are all intrinsically related and may lead to confounding of Plastic branching: capacity to form
attempts to establish which one is really decreasing leaf-scale carbon assimilation at the top of new branches from axillary
the tree. Plant size, not meristem age, has been considered as one of the major factors limiting meristems after a perturbation or
stress factor.
growth rates in trees. Using grafting experiments in Scots pine, it has been shown that relative Resilience: capacity to rebound
growth rates and net photosynthesis in leaves decline with increasing size irrespective of donor after a perturbation or stress factor.
tree age [27,28]. Furthermore, it has recently been shown that mutations occur at low rates in Resistance: capacity to avoid or
withstand/tolerate a stress factor.
the meristematic tissues of trees and other plant species [5,6,29]. Tree aging intrinsically leads
Senescence: negative effects of
aging on the physiology of the
organism (physiological senescence)
Box 1. Short- and Long-Lived Trees, the Human Being, and the Arts or the survival rates of a population
Short- and Long-Lived Trees (demographic senescence).
The category of ‘long-lived’ trees include those that live for over 100 years. Some of the oldest trees in the world are Stress: physiological process by
conifers, which outlive all other tree species on Earth and have lifespans of over 1000 years. A bristlecone pine (Pinus which a stress factor (see below)
longaeva) is the oldest recorded tree to date, with a current age of 5067 years (tree cored by Edmund Schulman, age limits growth at the cellular, tissue/
determined by Tom Harlan) [1]. By contrast, ‘short-lived’ trees are those that generally have a lifespan of less than 100 organ, or organism level.
years; many fall into the 25–50-year range. Short-lived trees include most varieties of palm, small ornamental trees, and Stress factor: any condition, either
fruit trees. Short-lived trees tend to be fast growing and small in stature and have less durable wood. biotic or abiotic, that limits growth at
the cellular, tissue/organ, or
Human Beings and the Arts organism level.
Although ‘supercentenarians’ (people who reach age 110 years) have been fully authenticated in 15 countries to date
[3], the greatest fully authenticated age to which a person has ever lived is 122 years (Jeanne Louise Calment, France).

Hans Baldung Grien (1484–1545) referred to the brevity of life for the human being in his painting The Three Ages of Man
and Death (Figure I).

In the painting, the artist also seems to show:

(i) that death is just a matter of time (with the hourglass);
(ii) the U-shaped mortality curve for humans (death being directly connected to the child and the old woman but not
to the young woman);
(iii) the tremendous diversity in maximum lifespans of species in the tree of life.
Interestingly, the painting includes a long-lived tree and an owl, both showing signs of senescence.

Is this observation scientifically correct? Are all organisms, even long-lived trees, subject to the inevitable effects of time?
What are the limits to mortality in long-lived trees? What do we know now, 500 years later, about this?

986 Trends in Plant Science, November 2018, Vol. 23, No. 11

Figure I. The Three Ages of Man and Death by Hans Baldung Grien.

Trends in Plant Science, November 2018, Vol. 23, No. 11 987

to increased height which, due to the related stress factors, is ultimately limited, irrespective of
the fact that the aging of the meristem is not associated with its failure [5]. Reproduction, which
is also intrinsically related to the size and age of trees, also plays a role in decreasing the relative
growth rates of mature individuals relative to those of juveniles, at least in part through increased
abscisic acid content [30]. Abscisic acid not only triggers plant response to water stress and a
number of pathogens, but also modulates plant growth generally leading to reductions in the
aboveground biomass growth [31]. Furthermore, reduced cytokinin supply from roots to
shoots through the hydraulic system could also limit growth rates in trees [32]. Therefore, it
appears that leaf-scale carbon assimilation and relative growth rates at the top of the tree may
be limited by factors that are extrinsic to the meristematic tissues such as plant age and height,
which lead to hydraulic and mechanical constraints and interact with biotic/abiotic stress
factors. All of these factors together, rather than any of them individually, ultimately determines
the functional diversity of the leaves found in the canopy.

Certainly, there are well-known hydraulic limits to tree height, but they do not reduce continued
vigorous growth lower in the tree, at least in some long-lived species. Intensive measurements
(averaging >7000 structural measurements per tree, supplemented with tree-ring measure-
ments from increment cores at different heights along the trunk) show that mass growth rates
for the world’s tallest angiosperm, tallest gymnosperm, and most massive tree species all
increase continuously with tree size [12,14]. The biggest trees are no longer getting taller, but
some sequoias are adding nearly 1 t of wood per year, increasing their girth and branches. A
global analysis suggested that increasing mass growth rate with tree size is a general phe-
nomenon [13]. It is therefore important to explicitly make the distinction between individual leaf
photosynthetic activity near the top of a tree and whole-tree mass growth. While carbon fixed
per unit of leaf mass and relative leaf growth rates generally decline with tree size, whole-tree
mass growth continues to increase because trees’ increase in leaf mass outpaces declines in
carbon fixed per unit of leaf mass [13].

It is well established that trees grow tall where resources are abundant, stresses are minor, and
competition for light places a premium on height growth [33]. Using data from the International
Tree-Ring Data Bank website and tree cores collected in the field, growth was found to increase
with age in eight tree species in the eastern USA [34]. Interestingly, however, the oldest tree
individuals in each species had consistently exhibited slow growth throughout their lives,
implying an inverse relationship between growth rate and longevity (Figure 1). This is consistent
with the idea that the longest-lived individual trees are generally found in places where
resources are scarce and environmental stress factors limit growth rates but with little compe-
tition from other organisms, as occurs with the oldest bristlecone pines recorded thus far [1]
and other woody polycarpic plants [35]. How is it therefore possible that abiotic stress factors,
such as water deficit, strongly limit tree growth and at the same time promote longevity? What
strategies allow some long-lived trees to survive for millennia?

Secrets of Long Life and Its Limits

‘You can’t get too much of a good thing’, the cliché goes. It is just as true that severe stress not
only reduces growth but may also eventually lead to death. Therefore, mild to moderate stress
may promote longevity in long-lived trees but severe stress may cause their death. The major
cause of temperate forest decline is severe biotic stress. Biotic factors (mostly insects and
pathogens) triggered mortality in 58% of the cases, and particularly in larger trees (86%), in a
survey of 3729 individual tree deaths recorded over a 13-year period in the coniferous forests of
the Sequoia and Yosemite national parks in Sierra Nevada, CA, USA [36]. In other words, biotic
stress is the major cause of mortality in such trees, particularly in mature individuals, a fact that

988 Trends in Plant Science, November 2018, Vol. 23, No. 11

 Indeterminate growth
Size
Determinate growth

(A) (B)
Size Longevity

Age
Growth
Stress

Age

Figure 1. Age–Size Relationship in Individuals with Determinate and Indeterminate Growth. (A) Age, size, and
stress are all interconnected factors governing, and ultimately limiting, growth. (B) Reduced growth rates have been
associated with increased longevity in trees.

has also been observed in several other studies including various tree species and the biotic
stress factor in the analysis [37–41]. Those studies also show that annual mortality rates range
between 1% and 3% in forests where biotic stress alone is the main driver of mortality, but when
it occurs concomitantly with severe drought, annual mortality rates rise to 10–30% depending
on the plant species and study site (for reviews see [42,43]). Therefore, biotic and abiotic stress
resistance and resilience are needed for long life in trees. Life expectancy and half-life for
trees and other polycarpic plants growing in their natural habitat is extremely low compared
with their maximum lifespans [35,44]. This means that only a very few individuals can survive for
long enough to reach advanced age, considering the maximum lifespan for long-lived trees.
From these considerations, we know that: (i) reaching an old age is an exception, not the rule, in
long-lived trees; (ii) senescence simply cannot be gauged in long-lived trees growing in their
natural habitat, because of the extremely low sample size in the oldest age groups; and (iii)
senescence does not seem to occur in long-lived trees in nature. Millennial trees could simply
be considered outliers in a given population and plant species. What is it that makes them so
special? How can they escape the wear and tear of aging?

Several features make millennial trees extraordinary in terms of longevity (Box 2). Besides their
slow rate of mutational changes, which is important to reset the system at the molecular level in
stem meristematic cells and allow new reiterations free from mutational defects [5,6], it is further
essential to consider structural aspects that optimize this feature. Tree age, height, and size are
intrinsically associated during tree growth and development (Figure 1). Age per se is usually
considered negative, but it is essential to reach a minimum size and height that helps the tree: (i)
withstand environmental stress at very early stages of development [45]; and (ii) reach com-
petence for first flowering and consequently attain the mature stage in plant development [46].
Size and height in mature, tall individuals can limit photosynthesis and relative growth rates, but
long-lived trees with extreme longevities extend their growth phase by increasing stem width
[13], thus prolonging indeterminate growth and preventing senescence of the entire organism
[16]. Additionally, I suggest that long-lived trees may take advantage of profound changes in
their structural organization at very advanced ages, which may be essential to reach extreme
longevity. In bristlecone pines and olive trees, multiple (in space and time) shoot reiteration from

Trends in Plant Science, November 2018, Vol. 23, No. 11 989

 Box 2. How Millennial Trees Withstand Aging and Their Limits
Slow Rate of Mutational Change
A key feature of extreme longevity in long-lived trees is the low rate of mutational change achieved by new meristematic
iterations. If stem cells divide only a few times, the chance of suffering deleterious mutations may be low. The mosaic-
like organization of meristematic growth points in trees also contributes to reducing the potential negative effects of
mutations, since the individual will not suffer from the effects of aging even if a few of the individual ramets fail to survive.

Limitation

The adaptation of long-lived trees to a broad range of conditions can be limited by a slow rate of mutational change;
hence, long-lived trees will be found only in very restricted areas, usually under conditions of abiotic stress but therefore
with little competition from other organisms and reduced biotic stress (Figure I).

Growing on Dead Structures

One of the ‘secrets’ of long life in long-lived trees is a dramatic reduction in the proportion of living structures relative to
total biomass while keeping the vascular system intact. This is achieved by simply constructing new life on top of dead
tissue, while the development of the secondary phloem persists in trees.

Limitation

Biotic stress on the vascular system strongly limits the longevity of trees.

Resetting the System

A long-lived tree is like a community (genet) formed by a population of new reiterations (ramets). Even if all of the ramets
die, some meristematic points that have remained dormant for centuries can give rise to a new ramet and reset the
whole system.

Limitation

This resetting is again limited by the functionality of the vascular system. If the vascular system fails at some point
between the roots and the new iteration point of the aboveground part of the tree, even a long-lived tree will
inevitably die.

Figure I. Insects and Other Biotic Stresses Strongly Limit Tree Longevity.

axillary meristems (as a result of loss of apical dominance) may help in reaching extreme
longevities. As explained above, tree height and size limit growth upwards. Therefore, the
development of new axillary meristems leading to new multiple layers of apical control may help
to reduce the effects of maximum height and size on relative growth rates and may be an
effective way for mature trees to reach extreme long life without the need to increase further the
width of the main stem. It remains to be studied whether this is a programmed process, but I
suggest that resetting the system and growing from axillary meristems found in the lower part of
the canopy that have remained dormant for centuries appears to be an efficient means of
reaching extreme longevity.

990 Trends in Plant Science, November 2018, Vol. 23, No. 11

The plasticity of millennial trees is tremendous. They slough off the limitations on relative growth Outstanding Questions
rates of increased height and size and their mortality is limited only by biotic and abiotic stresses Are long-lived trees potentially
and by spatial and structural constraints, which are strongly species and site specific. However, immortal?

competition for space is one of the most important, sometimes overlooked, causes of mortality in
What are the limits to longevity in long-
trees [45–47]. Millennial trees are usually found in isolated sites with little competition. Meanwhile, lived trees?
resistance and resilience in trees are usually shaped by the effects of competition, which may
influence growth performance and death even more strongly than climate, an aspect that has been Do long-lived trees show symptoms of
particularly studied in juvenile individuals [48,49]. Interestingly, drought responses may be signifi- senescence?
cantly influenced by tree age: older trees are more resistant but less resilient than younger
Are reduced rates of growth related to
Pseudotsuga menziesii trees [49]. Millennial trees appear to be an exception to this rule, being
extreme longevity in trees?
both resistant (like old trees) and resilient (like young trees), as they escape from the negative
effects of increased height and size and are capable of resetting the system.

Despite the tremendous plasticity of long-lived nonclonal trees, millennial trees are not immor-
tal. As mentioned above, a slow rate of mutational change, the capacity for slow but continuous
growth, and plastic branching may serve as a means to reach extreme longevities in some
nonclonal trees, but even in these millennial organisms immortality can be attained only through
the germ line. Structural limitations associated with a failure to reconnect the vascular system to
communicate between roots and shoots during resetting, or very severe biotic/abiotic stresses,
will cause the death of millennial trees (Box 2). It appears that global change is increasing
mortality in millennial African baobabs, the longest-lived nonclonal angiosperm trees [2].
Furthermore, enhanced resistance to biotic stress explains, at least in part, the greater longevity
of centennial oaks compared with other, short-lived angiosperm tree species [50]. Therefore, it
appears that genetic factors influence species and interindividual differences in longevity, thus
paving the way to study the genetic factors underpinning biotic and abiotic stress resistance
and resilience in millennial trees, an aspect that warrants further research. Despite the advan-
tages provided by unique genotypes, death (as an individual) is inevitable for all living organ-
isms, even for the still-living millennial trees, as immortality can be attained only through the
germ line or using clonal propagation, which loses the individual entity.

Concluding Remarks and Future Perspectives

Growth and longevity are interconnected: reduced growth rates during early life increase
longevity in trees and, most importantly, continuous growth, even at low rates, prevents
senescence occurring. Interestingly, millennial trees keep their growth capacity intact, at least
in some plant parts. With their extreme longevity, millennials illustrate the tremendous plasticity
of perennial plants and pose a threat to our current understanding of aging. Biotic and abiotic
stresses are the major causes of mortality in forests but at the same time will lead to reduced
growth in the more resistant and resilient individuals, thereby acting as a selection pressure on
tree communities with long-lived individuals. After attaining maximum height and size, the tree
will show maximum vigor but will still be exposed to extrinsic factors that could cause its death.
However, a slow rate of mutational change and the capacity to reset the system after a loss of
apical dominance may be essential key features of extreme longevity. Despite cases of extreme
longevity in nonclonal trees, immortality in trees and other organisms can be achieved only
through clonal reproduction or by transmission of the germ line over generations through sexual
reproduction. In both cases, immortality is achieved at the cost of losing the identity of the soma
as a unitary form of life. The mechanisms used by millennial trees are not a perfect system for
the soma to reach immortality but are close to this. It should be noted, however, that this
strategy is based on a complete renewal of all organs and cannot be afforded by other
organisms, such as humans (at least to date), due to a completely different genetically driven
developmental program.

Trends in Plant Science, November 2018, Vol. 23, No. 11 991

Acknowledgments
Research in S.M-B.’s laboratory is supported by the BFU2015-64001-P/MINECO/FEDER grant from the Spanish
Government and the ICREA Academia award funded by the Generalitat de Catalunya regional authorities. I thank my
son Gerard for helping me find some inspiration in the arts, as well as all my present and past laboratory members and
other colleagues in the field, for helping me to find some inspiration in science. I also greatly appreciate comments and
suggestions made by Toffa Evans, Susanne Brink, Larry D. Noodén, Roberto Salguero-Gómez, and one additional
reviewer on earlier versions of the manuscript.
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