This is the transcript of a talk I gave on 2010.06.11 at the Pinetum Blijdenstein (Netherlands), at the release of Aljos Farjon's new book, A Handbook of the World's Conifers. It discusses the biological basis of longevity in conifers, and presents some of the oldest known trees.
My thanks to Aljos for inviting me here, Brill for their support, and the Pinetum for providing such a lovely venue for this meeting. I’m here because of Conifers.org. In this capacity my work with conifers is primarily that of an enthusiast and an educator; conifers are not central to my work as a scientist. However, since the 1970s I have worked with many respected researchers who are on the cutting edge of conifer science in fields such as ecophysiology, forest ecology, dendrochronology, and plant systematics. In today’s presentation I have attempted to synthesize that experience to provide a broad overview of current scientific understanding of conifer longevity.
Today’s talk is going to be divided into two roughly equal parts. First I will discuss some aspects of the biology of conifer longevity. I will try to keep this general, but any discussion that addresses cell biology and genetics is apt to get a bit technical, for which I apologize in advance.
Second I will present a survey and review of the oldest conifers, by which I mean, the species that are represented by living or recently living trees over 1000 years old. The number 1000 years has no special significance, unless you use a base 10 number system; but since this left me with 25 taxa, it seemed a convenient number for this talk.
Much of my discussion of tree biology harps on the theme that trees are not animals. This seems obvious, but in fact, both lay people and scientists often treat them as if they were animals, even to the point of anthropomorphizing them. In this connection I would like to plug a wonderful book called In Praise of Plants by Francis Hallé, which shows how plants differ from animals, how little traditional biologists understand that fact, and how profoundly it can affect our understanding of botany. Let’s look at how that affects our understanding of tree age.
There’s a long list of fundamental differences between plants and animals. A few of them are closely relevant to the problem of tree longevity.
First, there is no continuity of germ plasm. Many plant cells have the ability to create a new plant – a fact that we use all the time when we propagate plants from cuttings. In general, new growth occurs from undifferentiated cells in the meristem tissues, which occur in the cambium as shown here, or at growing tips of stems or roots.
Second, plants are modular, capable of an indeterminate number of leaves, or stems, or roots, in response to environmental changes. To a large degree these modules are independent of each other: most of the time the death of a leaf, or stem, or root does not have awful consequences for the rest of the plant. Think of the difference between cutting a limb off an animal and cutting one off a tree. To some degree, trees can be thought of as colonial organisms. How old is a colony?
The colony analogy is revealed in another way: trees basically consist of a dead woody core of heartwood that serves to provide structure for a veneer of living tissue. Only the veneer is alive, but when we speak of a tree being old, we usually mean that it has an old woody core.
One consequence of this modular and colonial growth strategy is that our perception of a tree as an individual is illogical; it is another instance of zoocentrism. To the tree, an individual woody structure is only important insofar as it provides a competitive advantage by providing an extensive root system to gather nutrients and water, or height growth that allows greater access to sunlight. If circumstance allow, the colony can easily appear as many individuals. For example, there are examples of yew trees that are thought of as being over 1000 years old because a yew tree has been growing in the same place for 1000 years; yet there may be several distinct stems, each of which has no living cell over 100 years old, and there may be no remnant of wood that is over 500 years old. How old is that tree? It depends on what you call age.
One way to think of a tree’s age is to consider the age of the oldest living cells. You don’t often see this number, which by the way is not more than 150 years. The subject is rarely mentioned in the literature and I haven’t seen that it has been studied very much with regard to systematics or ecology.
Sapwood is xylem that contains living cells. The oldest living cells in a tree are therefore found in the oldest part of the sapwood. They are called ray parenchyma cells, and their principal purpose is to convey materials from the phloem and cambium to the sapwood/heartwood boundary, where antifungal compounds are deposited to form the tree’s heartwood. The oldest recorded sapwood is about 150 years old; therefore the oldest individual living cells in a tree are also about that age. In most trees, though, the sapwood is much younger.
A second way to think of the age of a tree is to consider the age of the dead woody core. This is what people usually mean when they speak of a tree as being old.
The age of the wood core is often easy to measure, and has been studied extensively. The oldest known examples are between 4,000 and 5,000 years. In most of this talk, I will be discussing age of the dead woody core of a tree.
A relatively recent discovery is that the dead woody core of the trunk can be much, much older than any of the branches or limbs. This chart shows crown maps of Pseudotsuga menziesii; the trees on the right are about 600 years old, and nearly all of the existing branches are epicormic, that is, they have arisen since the tree grew to approximately its current height. Work with species such as Sequoia and Sequoiadendron has shown that a tree may lose primary structural branches six or seven times over the course of its life, each time regenerating new branches of similar size and structure. Thus the shape of a tree’s crown can change dramatically and repeatedly over its life.
Finally, we can think of the age of tree as being the age of a genet: the time span since that organism’s genes were recombined through the process of sexual reproduction. This numberis usually difficult to measure but is important when considering trees that form long-lived clones, like Huon pine (Lagarostrobos franklinii). Ages of such clones have been reported to exceed 10,000 years. Extremely old genets are also common in Sequoia and Taxus. The age record, though, belongs to the angiosperms: 43,600 years for a Lomatia tasmanica clone that, ironically, grows in the range of Huon pine.
One of the oldest known tree species that does NOT have an old dead woody core is Taxus baccata. It is the only such species I’ll talk about today. According to some authorities, the largest and perhaps oldest example is the Fortingall Yew in Scotland, shown here. At some time in the past it presumably had a single trunk and crown, but as it has grown, the heartwood has decayed and it has split to form multiple crowns that nonetheless represent a single genetic individual. The drawings here show how much the tree’s appearance has changed in the past 270 years; how much more might it change in a millennium? Clearly there is no way to tell the age of such a tree simply by inspection of the surviving plant.
Now I’d like to spend some time talking about how and why trees die. The message here is that unlike animals, trees don’t die of old age: they die because something kills them.
The principal causes of mortality are competition, fire, insect attack, human activity, and fungal attack. There are many others (wind, flood, landslide, etc.).These are not necessarily independent causes; for instance, an insect attack that kills many trees in a stand may leave the entire stand vulnerable to fire.
The ultimate enemy of wood, though, is fungus. If nothing else kills a tree first, it will succumb in the end to fungal attack.
All old trees that are nearing the end of their life show evidence of decay caused by fungi. These fungi, such as the common stem rot Phaeolus shown here, or the common root rot Phellinus, usually enter the tree from the ground or from an injury such as a broken top or fire scar, and they slowly decay the heartwood and roots.
This fate is so inevitable that most conifers devote a substantial part of their entire energy budget to producing antifungal compounds and sequestering them in the heartwood and around wounds.
The process of fungal attack may continue for hundreds of years and the effect is a gradual weakening of the tree. In the end, the tree usually dies by breaking off or uprooting.
Now I’d like to talk a little about senecence. Senescence is a physiological decline intrinsically related to the age of the tree. Briefly, this is another zoocentric concept that doesn’t seem to apply to trees. Connor and Lanner (1990, 1991) and Larson (2001) looked at Pinus longaeva and Thuja occidentalis for evidence of senescence, testing various factors that other researchers had hypothesized might be related to the process of senescence in trees. All tested factors produced negative results; that is, these properties were the same in the oldest trees as in young trees. There is an important caveat: comparable tests have not been done for unquestionably short-lived conifer species, and indeed the subject has not been looked at with regard to most tree species.
This result begs the question: is there evidence of a genetic basis for tree senescence? The problem is still not well understood, but some recent studies are relevant.
Telomeres are structures at the ends of the chromosome that play a critical role in cell division. Organisms with longer telomeres can sustain more cycles of cell division, and organisms with higher activity of the enzyme telomerase can better repair shortened telomeres.
Pinus longaeva has significantly longer telomeres and higher telomere activity than more short-lived pine species (P. taeda, P. palustris, P. resinosa). Watson and Riha (2010) note that “the rate of molecular evolution in trees and shrubs with long generation times is slower when compared to related herbaceous plants with shorter generation times ... One explanation for this observation is that plant meristematic cells possess robust DNA repair and genome maintenance mechanism.”
Interestingly this is an active research area among genontologists, seeking to discover ways to use plant genes to make humans live longer.
Now we’re going to consider some data pertaining to the 25 conifers that have been shown to have dead wood cores more than 1000 years old.
The longest-lived tree species have two genetically-controlled traits that confer resistance to fungal attack. First, all of the longest-lived trees produce wood that has a high content of often highly aromatic compounds that are highly resistant to fungal attack. This trait is especially common in the Cupressaceae, but also appears in the oldest species of Araucariaceae and Pinaceae.
Second, eight of the longest-lived species also grow rapidly to a very large size. Other things being equal, it will take longer for fungal decay to destroy the structural integrity of a large tree, and typically these very large trees display evidence of extensive fungal decay of heartwood when they are finally felled by natural causes such as windthrow. In these eight species, size and age show a fairly good correlation, a relationship that is NOT generally the case amongst very old trees.
Now let’s consider climate and its relationship to longevity. All of the oldest trees live in temperate areas. Only Agathis australis and the two species of Taxodium are also represented by very old trees in subtropical climates. Nearly all live in habitats that are exceptionally wet (11 of 25 taxa) or exceptionally dry (10 of 25 taxa); of the latter, 6 taxa moreover experience exceptional cold. Only four taxa live in mesic, low to montane habitats: Sequoiadendron, the two species of Taxodium, and Thuja occidentalis. The first three live on very wet sites that never experience drought and thus create a physiological environment similar to rainforest. The Thuja only attains great age on limestone cliffs where it suffers severe physiological drought most of the time.
This choice of habitat correlates with reduced risks of fungal attack and decay. Aridity and cold clearly reduce fungal activity. Fungal decay in rainforest settings is slowed by saturation of the heartwood which produces an anoxic environment, discouraging fungal decay of heartwood. Also, the oldest rainforest trees have a high level of productivity which allows them to devote a large fraction of their resource budget to combatting fungal attack.
I’ll sum up here with some rules of thumb about where to find the oldest trees.
If a species grows in an arid habitat, the oldest individuals will be found there. Trees in arid habitats tend to be widely-spaced and short in stature, so they have a low risk of windthrow or insect attack, and the stands often do not have enough biomass to carry a fire. The slow growth rate means that the tree rings have a high latewood content, thus a higher content of lignins, which are resistant to fungal attack. Also, fungal activity is reduced in the arid environment.
If a species grows as a dominant in a closed-canopy forest, the oldest individuals will tend to be the largest. In such a forest, trees that avoid other causes of mortality will eventually be felled by root or stem rots. Large and vigorously growing trees have more resources to defend against fungal attack and will thereby live longer than their smaller, less-vigorous competitors.
Among species in forests with gap-phase regeneration dynamics, the oldest trees will be those canopy trees that formerly spent extended periods in suppressed growth as shade-tolerant sub-canopy trees. These trees produce a very dense, lignin-rich wood during their suppressed growth period, which protects them from fungal attack. They may succumb to root rots during this period, but if not, may be several hundred years old by the time they enter the canopy and start to act as canopy dominant trees.
For the remainder of the talk I’ll be briefly reviewing the oldest known trees. There is much to say about each of these species – and little time to say it. I will focus on age-related information, and we can cover other topics during questions.
We’ll first treat species in rainforest (or otherwise wet) habitats.
The largest and presumably oldest trees in New Zealand have only been shown to live about 800 years, but all of the oldest ones have extensive heartrot and trees much larger than any now living were logged in the historical period. Ages likely exceed 1000 years. Nonetheless, this is the most short-lived species on the list.
The oldest known age is a ring count of 1065 years for a stump, from Yakushima Island, Japan. The tree shown here, of var. formosana in Taiwan, has been cored and crossdated to yield a minimum age of 1006 years. Substantially larger and presumably older trees are known.
The oldest known tree, shown here, grows in a marsh and has a crossdated age of 1140 years. Many trees over 3 m diameter are known and all grow in wetlands or atop springs. One has the largest base of any known tree and is likely several thousand years old. Extremely rot-resistant wood.
This is the tree at Santa Maria del Tule in Oaxaca. It appears much older than any sampled specimen of this species, but its age is quite unknown.
The oldest known tree had a ring count of 1460 years. All of the very large trees have extensive heartrot and many are over 5 m in diameter, so the maximum age is likely much greater but cannot be determined.
The oldest tree, 1622 years, lives in a blackwater swamps in North Carolina, is nearly 3 m in diameter, and is quite hollow. Old trees usually lose their tops in hurricanes, and this probably fosters decay of heartwood.
The oldest tree was a ring count of a tree logged in the 19th Century on Yakushima Island, Japan. Yakushima is the wettest place in Japan, with 7 m of rain a year, and contains many Cryptomerias 2 to 3 m in diameter. The wood is extremely rot-resistant.
The oldest specimen has 1834 rings. Again, the oldest and largest trees have extensive heartrot.
Ages of over 2200 years have been recorded for this, the tallest and formerly the largest conifer on the planet. The tree shown here, cut in 1945, was the largest tree ever measured. It had extensive heartrot and yielded little commercially usable wood. This species typically regenerates from stump or root sprouts; some genets may be as much as 10,000 years old.
With ages to 3266 years, it is the 3rd oldest species. It has the thickest bark of any tree and is almost perfectly fireproof. A fire can torch the tree, burning off all living foliage and smaller branches, and the tree will resprout from the bark and redevelop a normal crown. Severe drought can cause the same response. Growth is so rapid that it appears to swamp the ability of a fungus to produce any substantial structural weakness; death appears to principally result from fires that burn through the bark and smolder within for long enough to consume the tree.
The McKinley Tree shows how the species is normally emergent, with the live crown mostly exposed to sunlight. Productivity is not limited by light. Nor is it limited by water. The groves all grow in areas with shallow groundwater and tree-ring evidence suggests they are rarely drought stressed. The Boole tree lost most of its live crown when the surrounding forest was logged, but has epicormically resprouted as a new Sequoiadendron forest has grown around it. Such loss and regrowth of branches likely occurs repeatedly over a tree’s life and allows a dynamic response to changing water and light availability, while also facilitating recovery from fire.
The second-oldest tree, with verified ages of up to 3622 years. The “austral redwood,” it grows to huge sizes and has an extremely decay-resistant wood.
One subspecies of Pseudotsuga menziesii lives to great ages in the rainforest; the other, in the desert. This is the rainforest subspecies. The oldest trees exceed 1000 years and the record is 1350 years for a tree felled by stem or root rot on Vancouver Island.
With ages to about 1400 years, this is the best example of a tree that attains great age by spending centuries as a suppressed understory sapling, before entering the forest canopy to spend 600 years or so as a canopy dominant tree. A similar strategy is found in several other temperate rainforest species that are not yet known to exceed 1000 years.
Ring-counted ages of 1200 years are known for the oldest of New Zealand’s rainforest podocarps. Very old trees may have little heartrot, prompting the question, do they have exceptional antifungal compounds, or does New Zealand lack some of the more effective root and stem rot fungi? I do not know that the question has been studied.
>The Huon pine lives in Tasmanian rainforests, often in riparian settings; it has an extremely rot-resistant wood. The most ancient stand is a clone, possibly over 10,000 yrs old.
Finally we will review the 11 taxa living in semiarid climates, six of which are moreover confined to high, cold mountain settings.
Ring-counted ages of 1300 years have been reported. Although the largest trees grow in fairly mesic settings, the oldest ones are on drier sites and in locations that are less vulnerable to high-intensity fire.
This species has been used extensively in dendrochronology. The oldest tree ever found, shown here, yielded a record 1600 years long. Many trees over 1000 years old are known. The species is not protected and, in an ongoing management travesty, extremely old trees are regularly killed to enable more extensive livestock grazing on public lands.
Although the celebrated arborvitae is usually a relatively short-lived forest tree of the eastern United States and Canada, it also occurs on dry dolomite cliffs of the Niagara Escarpment. Ages of up to 1653 years have been demonstrated for these trees, and substantially older trees may yet be found.
J. scopulorum is very nearly the same species as J. virginiana, and the two comprise the most widespread juniper species in the New World. The very oldest trees are from very arid, rocky sites, where ages of up to 1888 years have been found.
This is the oldest and, many would say, the most picturesque of all the junipers. It has a maximum age of 2675 years. It was about that long ago that Chuang Tzu put forth his theory of old trees. He wrote “Its trunk is too gnarled and bumpy to apply a measuring line to, its branches too bent and twisted to match up to a compass or square. You could stand it by the road and no carpenter would look at it twice. ... Axes will never shorten its life, nothing can ever harm it. If there's no use for it, how can it come to grief or pain?”
The oldest verified age is 1267 years for a tree collected in central Idaho. Although it grows in mesic to arid high mountains, the oldest trees are from the driest sites. This tree was about 1000 years old, and grows in the Independence Mountains of Nevada.
This subspecies of Pseudotsuga menziesii has an enormous range, from Alberta to Oaxaca across 36 degrees of latitude. The oldest trees known, up to 1275 years, grow on lava flows in a desert region and thus suffer extreme drought stress.
The oldest confirmed age is 1670 years. The oldest trees occur on arid, rocky sites, often on carbonate substrates. The species often co-occurs with Pinus albicaulis, but generally occurs on drier, rockier microsites.
The oldest three pines belong to section Balfourianae and are extremely genetically conservative, closely resembling fossils that date to more than 60 million years ago. This is the youngest of the three, with confirmed ages to 2110 years. It lives in cold dry alpine settings, rarely below 3000 m elevation, and has an extremely resinous wood.
The oldest verified age is 2435 years. The oldest trees have been found on the highest and driest sites. Like the two other pines in section Balfourianae, the ancient trees of this species are predominantly killed by lightning strikes, rather than by fungal attack.
The oldest of all trees at 4844 years, Great Basin bristlecone pine lives in a cold dry alpine setting and has extremely dense, resinous wood, commonly with 200 rings per inch. Trees over 2,000 years old are very common. Decay is uncommon; the wood of dead trees sometimes rots but often is just eroded by windblown sand and ice crystals, and pieces 10,000 years old can be found lying on the ground.
Connor, K.F. and R.M. Lanner. 1990. Effects of tree age on secondary xylem and phloem anatomy in stems of Great Basin bristlecone pine (Pinus longaeva). America Journal of Botany 77:1070-1077.
Hallé, Francis. 2002. In Praise of Plants. Portland, OR: Timber Press.
Lanner (1991) [pending]
Larson, D.W. 2001. The paradox of great longevity in a short-lived tree species. Experimental Gerontology 36(4):651-673.
Watson, J.M. and K. Riha. 2010. Telomeres, Aging, and Plants: From Weeds to Methuselah - A Mini-Review. Gerontology 4:327-338.
Thanks for the use of illustrations:
Gymnosperm Database pages for each of the species mentioned herein.
Briand, C.H., U. Posluszny and D.W. Larson. 1993. Influence of Age and Growth Rate on Radial Anatomy of Annual Rings of Thuja occidentalis L. (Eastern White Cedar). International Journal of Plant Sciences 154(3):406-411.
Flanary, B.E. and G. Kletetschka. 2005. Analysis of telomere lengthand telomerase activity in tree species of various lifespans,and with age in the bristlecone pine Pinus longaeva. Biogerontology 6(2):101–111.
Kelly, P.E., E.R. Cook, AND D.W. Larson. 1992. Constrained growth, cambial mortality, and dendrochronology of ancient Thuja occidentalis on cliffs of the Niagara Escarpment: An eastern version of bristlecone pine? Int. J. Plant Sci. 153:117–127.
Lanner, R.M. and K.F. Connor. 2001. Does bristlecone pine senesce? Experimental Gerontology 36:675-685.
Spicer, Rachel. 2005. Senescence in Secondary Xylem: Heartwood Formation as an Active Developmental Program. Pp. 457-475 in N. Michele Holbrook and Maciej A. Zwieniecki (eds.), Vascular Transport in Plants, Academic Press, Burlington.
The Powerpoint for this talk is available HERE (right-click and choose "save as" ... 21 MB file).