Initial online release 3/2/2000; updated 12/20/2002
While it is true old oaks die, oaks do not die simply of old age. An oak contends with a wide variety of plant pathogens and insect pests throughout its lifetime, and more often than not, it is these natural enemies which finally cause the demise of the "sturdy oak". Oaks fight a seesaw battle with these minute adversaries, sometimes gaining, sometimes yielding ground. The interplay between oaks and their natural enemies provides a classic illustration of the natural balance that exists between different organisms, and how human activities can destroy this balance. In this paper, we will highlight the important role that pathogenic microorganisms and insects play in the ecology of California's oak woodlands.
We originally discussed this topic in a 1990 paper before the rise of sudden oak death, a canker disease caused by the pathogen Phytophthora ramorum. The changes wrought by this pathogen in affected woodlands has prompted us to revise and update our discussion in this paper. Although P. ramorum has had substantial impacts in some oak woodlands, it is important to remember that most oaks in California have not been affected by this pathogen. Even in areas that are affected by sudden oak death, this new disease functions in a woodland matrix that includes a variety of native pests and diseases. We cannot hope to understand how to deal with this new disease without understanding the broader picture of plant health in the affected woodlands and forests.
Like other plants, oaks have developed a variety of biochemical and physiological defenses to resist attack by pests and pathogens. The level to which these defenses are expressed may vary between different oak species and even among the individuals of a single species. These defense mechanisms may restrict some microorganisms and insects to a single oak subgenus, a single oak species, or even to certain individuals within the species.
The resistance of oaks to diseases and insects is further influenced by the condition and age of the tree or its parts. Disease and insect impacts are often more severe on stressed or slow-growing trees, because such trees have a reduced ability to defend against or compensate for injury or disease. Many of the wood-boring beetles, for example, only colonize stressed branches or trees. Conversely, some agents preferentially attack the lush growth of vigorous trees. Powdery mildew often occurs on young, succulent blue oak stump sprouts, but is absent from the foliage of mature trees in the same vicinity.
Innate susceptibility is not the only factor that governs the severity of disease and insect impacts. Environmental conditions limit the distribution of various pathogens and insects, and strongly influence their rates of growth and reproduction. Due to environmental differences, certain disease and insect impacts may be quite severe in some parts of an oak's range, and negligible in other parts. Furthermore, changes in environmental conditions from year to year can also influence oak growth, vigor, and stress as well as pathogen or insect populations. Perturbations in weather patterns can sometimes change the intensity of disease and insect impacts over wide areas. For example, a drought may stress oaks over a wide area; a wet spring, with frequent rains falling over an extended period, can increase the intensity of leafspot and twig canker diseases.
Disease and insect impacts on oak life stages
Insects and plant pathogens may attack oaks at any life stage, from acorn to mature tree, resulting in reduced survival and regeneration. Through a number of studies beginning in 1987, we have compiled quantitative information on how various diseases and insects affect the oaks of California's woodlands and savannas. Much of our recent work focuses on woodlands dominated by coast live oak (Quercus agrifolia) and black oak (Q. kelloggii) in northern California, whereas our earlier work focused primarily on blue oak (Q. douglasii) woodlands. Our findings are discussed below.
Although many California oaks are capable of vegetative reproduction by crown sprouting, reproduction by seed is more common in many locations. Reproduction from seed is also important ecologically, since it helps maintain the genetic diversity necessary for the species to adapt to changing conditions. Insects and diseases that attack acorns can affect seed- or seedling-based artificial regeneration as well as natural regeneration. To evaluate impacts of insects and pathogens on acorns, we dissected over 1000 acorns collected over two years from different areas.
We were initially interested in determining whether external symptoms could be used to assess the internal condition of acorns. We soon found that this is about the same as trying to judge a book from its cover. Many perfectly healthy acorns have oviposition and entry scars, or some superficial fungal growth. On the other hand, many acorns with extensive internal damage or decay show no obvious external symptoms. For a variety of oak species, we found that insect exit holes are the only reliable indicator of internal injury. The presence of one or more of these circular, 1-2 mm diameter holes normally guarantees at least moderate levels of internal damage, and planters would do well to cull out such acorns. Nonetheless, the absence of exit holes does not guarantee that an acorn is sound.
The larvae of two insects, filbert weevils (Curculio spp.) and the filbertworm (Cydia latiferreana), account for almost all of the insect injury we have observed in both blue and valley oak acorns. The weevil larvae are legless, relatively sluggish, and roughly C-shaped when removed from an acorn. Filbertworm larvae have legs and are often quite active. When removed from an acorn, filbertworm larvae may drop down on a strand of silk. Contrary to a popular belief, acorns do not become infested by these insects after they drop. Acorns are colonized while they are on the tree, but insect development continues after the acorns have fallen. Usually only a single filbertworm larva colonizes an infested acorn, whereas up to five of the smaller curculio larvae can be found in a single acorn. Both species are sometimes found in the same acorn. We have seen that the relative abundance of each insect species, and the overall percentage of infested acorns varies location to location and year to year.
Damaged acorns tend to drop from trees early, often well in advance of normal acorn ripening. As a result, acorns collected from the ground normally have much greater levels of internal disease and insect injury than acorns collected from the trees during the same period. This is the main reason why acorns collected for planting should be picked from the tree rather than from the ground if possible.
Seedlings and saplings represent the next generation of oaks. The blue oak seedlings we have studied are quite small - mostly less than 10 cm tall, with 10 or fewer leaves - and would go completely unnoticed by the causal observer. The best view of these seedlings is obtained on one's hands and knees. Seedlings are attacked by many of the same insects that affect the foliage of overstory trees. Leafhoppers and various leaf-feeding caterpillars commonly affect both trees and seedlings, primarily in the spring. However, damage by insects is usually incomplete and spotty; one seedling may be nearly defoliated while another a few inches away will be unscathed. Overall, we found that foliar feeding by insects had no apparent effect on blue oak seedling survival. The primary factor affecting blue oak seedling survival in nongrazed areas was water stress. Heat and drought take a heavy toll on blue oak seedlings, and relatively few seedling leaves persist the entire growing season in dry sites.
Blue oak seedlings possess various adaptations that reduce their risk of mortality from damaging agents. The germinating seedling uses the substantial food reserves stored in the acorn to produce an impressively long and stout taproot. This taproot not only taps soil water to some depth, but also functions in food storage. Since most of their energy reserves are stored below ground, oak seedlings are capable of recovering from the loss of most or all of the shoot by resprouting from the base. These characteristics allow blue oak seedlings to persist for a number of years in a seedling size. These persistent seedlings are critical to the reproductive strategy of blue oak. Since adequate acorn production and conditions favorable for seedling establishment do not occur every year, the chances for effective regeneration would be greatly reduced without these persistent seedlings. Nonetheless, seedlings that experience shoot loss during successive growing seasons do not survive as long seedlings whose shoots remain intact. Presumably, this is due to the gradual depletion of carbohydrates stored in the taproot. Other factors that kill or damage the shoot repeatedly, such as grazing or frequent fires, can also lead to the loss of persistent seedlings in the understory.
In general, insect and disease impacts on saplings begin to approach those seen in mature trees. As stems become progressively more woody, they are invaded by twig and wood-boring insects. Cynipid galls are quite common on saplings, and branch cankers and wood decay sometimes occur on larger stems. Where oak saplings are growing under favorable conditions, insects and diseases typically do not cause significant mortality or obvious health impacts. However, when saplings are highly suppressed by overstory trees, these opportunistic pests and diseases can lead to decline and death.
All oak trees do die eventually. While oaks may be killed at any life stage, death of a mature oak tree tends to attract more notice than the demise of a seedling or sapling. Occasionally, mature oak trees may die very quickly, but such occurrences were relatively rare until sudden oak death arrived on the scene. It is more common for mature oak trees to undergo a protracted period of decline prior to death, wherein they "die for a hundred years". Recent data show that even trees with symptoms of infection by the "sudden" oak death pathogen often survive for at least several years. Nonetheless, compared with the typical rate of tree decline associated with other oak pathogens, decline and death associated with P. ramorum may indeed seem to be sudden.
Very few of the many hundreds of biotic agents that attack oaks can cause the death of a mature tree. Insects and pathogens that attack leaves and twigs sometimes cause conspicuous damage, but their effects are often of more concern to people than they are damaging to the tree. Defoliators can weaken a mature oak if they cause significant damage in several consecutive years, but this situation is uncommon. Even the best known and most serious oak defoliator, the California oakworm (Phryganidia californica), seldom if ever causes the death of mature trees. The amount of damage caused by the oakworm fluctuates dramatically from year to year, giving trees a chance to recover from its attacks.
Decline of mature oaks is usually associated with infection by various wood-decaying fungi in the trunk, major branches, and/or the root system. Many of these fungi gain entrance to oak trees by way of wounds, such as fire scars, broken branches, and pruning wounds. If the tree is able to wall off or compartmentalize infections caused by these fungi, the pathogens may be entirely contained and decay will be limited. However, many of the wood-decay fungi are able to breach the barriers produced by the tree, and progressively decay more and more of the wood. This back-and-forth battle between oak and pathogen may continue for a long time, the tree losing more ground year by year. Finally, deprived of its structural and water-conducting tissues, the oak may collapse under its own weight or desiccate in a period of high water demand. Thus, although the final demise of an old oak may seem to be rapid to the casual observer, this terminal event is often the culmination of disease impacts dating back many years.
Although many different fungi can cause wood decay, our studies have demonstrated that a group of wood-decaying pathogens known as canker-rot fungi are especially common in stands of blue oak and coast live oak. These include several species of Inonotus and Phellinus, which infect oaks through branch stubs or other wounds. Canker rot fungi are important pathogens of oaks in both natural and urban settings. In addition to causing wood decay in the heartwood and sapwood of living trees, these fungi can advance toward the outer surface of the tree, killing portions of the vascular cambium and bark and causing external lesions known as cankers. The cankers are variable in form, but often appear as exposed portions of decayed wood where the bark has fallen away. In comparison, cankers caused by P. ramorum and many other canker fungi are initiated at the outer surface of the tree in the bark and do not extend into the wood to any great extent.
Hypoxylon thouarsianum and related sapwood-rotting fungi attack oaks in yet another way. Fungi in this group colonize the bark of healthy trees and function as opportunistic pathogens of stressed oaks, including trees attacked by P. ramorum. H. thouarsianum can decay the sapwood of affected trees to depths of at least several inches.
Decay caused by heart-rot fungi such as Laetiporus sulphureus, the sulfur fungus, eventually lead to the failure of large branches or the main stems of oaks. Mature oaks are also killed or may fail due to infections by root-rotting fungi. Species of Ganoderma are important lethal pathogens of mature oaks in woodlands as well as oaks that are incorporated into urban landscapes. Armillaria mellea and Phytophthora cinnamomi are root pathogens that have seldom been seen affecting oaks growing under natural conditions, but are significant pathogens of urban oaks that are subjected to summer irrigation and stressed by other rootzone disturbances. However, Armillaria root rot may develop in trees affected by sudden oak death even in the absence of other disturbances.
While California's oaks have endured adverse natural forces for eons, they are a poor match for a relative newcomer to the area, human beings. While people can and do kill oaks outright for various purposes, it is the less obvious and often unintentional ways that oaks are destroyed that are pertinent to the topic at hand. The fine balance that exists between oaks and their insects and pathogens can easily be knocked out of kilter by various human activities, often resulting in the rapid decline of affected trees. While there are few if any cultural practices that will increase the longevity of a mature oak tree, there are a great many practices that can shorten an oak's life.
Examples of the most common detrimental practices can be seen in a typical attempt to incorporate existing naturally-occurring oaks into the landscape of a new subdivision or development. The aboveground parts of oak trees are wounded by pruning and collisions with vehicles and construction equipment. These wounds serve as entry points for various fungi that cause cankers and wood decay, and are attractive to some wood-boring insects as well. In addition to these visible wounds, much more serious damage is commonly inflicted to the roots of oak trees. Many of an oak's roots are relatively shallow, and extend well beyond the edge of the canopy. Being out of sight and apparently out of mind, oak roots are routinely destroyed by grading, trenching, and soil compaction. Loss of roots can subject an oak to severe stress, which increases its susceptibility to diseases and insects.
Other human practices can change the tree's environment in such a way that it becomes more favorable for diseases and insects. Irrigation and altered drainage patterns impose a drastic change in the soil environment. Since many soil fungi are more active when soils are moist, excess moisture during the normally dry summer can release a constraint that would otherwise keep many of the soil-dwelling pathogens in check. Natural biological control of oak diseases and insects may also be disrupted by the use of broad spectrum pesticides. Insecticides and fungicides can destroy beneficial microorganisms and arthropods, leading to an increase in pest and pathogen populations. Changes in the composition of the oak understory could also reduce populations of beneficial organisms, resulting in increased pest activity.
Finally, pathogens or insect pests may be introduced with plant material, soil, or even irrigation water. Container-grown landscape plants which are planted within the root zone of established oaks can be infected by soil-borne pathogens even if they do not show obvious disease symptoms. The root-rotting Phytophthora species such as P. cinnamomi are frequently introduced into the landscape via contaminated plant material. The combination of stress, favorable disease conditions, and introduced pathogens, brought together by human activities, has sent many a sturdy oak to an untimely end. "Why did this oak die?" is often less of a question than "How did this oak survive?" when dealing with existing oaks incorporated into developed areas.
Unfortunately, many people fail to make the connection between the disturbances initiated at the time of construction and the eventual decline and death of an oak. A mature oak can have a large quantity of stored food reserves, so that even severe impacts will not usually cause the tree to die immediately. Damage, stress, and harmful cultural practices may take many years to kill an oak, but once initiated, the process of decline is generally irreversible. The rate of decline may be slowed by discontinuing harmful practices, but wood decay and the loss of major structural roots cannot be reversed, especially in old oaks. An oak that is healthy at the time it is disturbed will usually survive much longer than a tree which is already colonized by decay fungi. Further, young trees have a much better chance of adapting to changes in their immediate environment than do older trees.
It is often difficult to assess the age of established oaks, because diameter growth is strongly affected by environmental conditions and stand characteristics. Trees of a given trunk diameter may vary widely in age. Furthermore, in some areas, many of the mature trees have developed through coppicing, i.e., from root crown suckers produced by trees that were cut down. This is especially common among live oaks, which were used widely for fuel in the late 1800's and early 1900's and sprout very vigorously when cut down. Although the trunks of such trees may be only 50 to 100 years old, the root crown area and major structural roots could easily be an additional 50 to 100 years older. Factor in the possibility that the original stump may have been invaded by decay fungi, and it is clear that sprout origin trees may be much less tolerant of additional disturbance than a seedling-origin tree of the same shoot age.
However, whether young or old, healthy or diseased, most oaks survive longest when left on their own. True long-term oak conservation requires that we do no harm in the first place rather than trying to apply technological "fixes" to damaged trees.
Oak enemies: Indigenous vs. introduced
Plant pathogens and plant-feeding insects that have coevolved with California oaks have attained a certain balance with their host plants through long association. This is not to say that these indigenous agents are unimportant. Many indigenous pests and diseases pose very serious limitations on the growth and reproduction of their host plants, and may limit species distribution much as soil type or environmental conditions do. However, because these agents are omnipresent, their effects may be overlooked. As we have discussed above, individual native diseases and insect pests may have effects on oak health and survival that range from negligible to major.
In addition to these native agents, California oaks must contend with exotic pests and diseases that have been introduced into the state through human activities. Many introduced oak pests, such as oak pit scales (Asterolecanium spp.), have become widely distributed throughout the state. When plants are subjected to introduced pests and diseases, they face an unknown enemy and may be ill-prepared for the battle. The outcomes of these conflicts are occasionally disastrous. Classic examples include the devastation of native American elms by Dutch elm disease and native chestnuts by chestnut blight. The introduced pathogen Phytophthora lateralis causes a lethal root rot of Port Orford cedar that has had significant impacts on this native forest species in California.
In the original (1990) version of this paper, we raised the prospect that an introduced disease or pest could have disastrous consequences for California's oaks. Starting in the mid-1990's, unusual amounts of tree death were observed in several species of California oaks and tanoak in many coastal northern California counties. In the summer of 2000, Phytophthora ramorum, a previously undescribed pathogen, was identified as the cause of the stem canker disease that was christened sudden oak death. Evidence from several lines of research indicates that P. ramorum was possibly introduced into both California and Europe (where it is now primarily a disease in nursery-grown rhododendrons and viburnum ) from a third unknown source. This disease provides a graphic example of how severe the impact of a novel pathogen can be in California's oak woodlands, and it may not necessarily represent the worst case scenario.
Regulatory measures, including inspections and quarantines, are being employed in an effort to stop the spread of P. ramorum. Similar regulatory control practices have been used for many years to exclude other known oak pests and pathogens, such as oak wilt, caused by the fungus Ceratocystis fagacearum, and gypsy moth (Lymantria dispar). It is difficult enough to try to exclude or contain known pests and pathogens, but how do we defend against the unknown? Our experience with the sudden oak death pathogen brings to light inherent weaknesses in our current regulatory control practices. If we hope to protect existing ecosystems from potentially invasive or damaging pests, pathogens, weeds and other organisms, we have to do a much better job of ensuring that exotic organisms are not spread around the globe willy-nilly through international commerce and travel. Even on a local scale, we need to realize that planting a diseased plant from a nursery in a yard adjacent to a forest has the potential to spread pathogens into a native ecosystem.
Injurious and beneficial insects and microorganisms have an important place in the ecology of California's oak woodlands. Decay fungi and wood-consuming insects assist in the recycling of nutrients needed to support plant growth. Many insects that utilize oaks are fed upon by other insects, as well as birds, reptiles, and mammals that inhabit the woodlands. Acorn woodpeckers and a variety of other cavity-nesting birds and animals depend on the hollows and decayed branches produced by wood-decay fungi. Decayed branches which break and fall to the floor provide shelter for numerous animals. When viewed in the context of oak woodland ecology, most plant pathogens and oak-eating insects are neither "good" nor "bad", they are simply parts of the whole ecosystem.
Unfortunately, the expansion of urbanization and other intensive land uses have chopped oak woodland ecosystems into smaller and smaller fragments, threatening the integrity of the ecosystem. People build among the oaks in order to enjoy the natural beauty of these wonderful trees, and immediately (and often unconsciously) begin to destroy the oaks that surround them. Instead of regenerating local oak populations, which may possess unique genetic resources that are especially adaptive to the area, large container-grown "native" oaks of unknown seed origin are transplanted into close proximity with existing woodlands. These alien "natives" can not only serve as a source of introduced pathogens and insect pests, but can also serve as a source of "genetic pollution" that can adversely affect the genetic makeup of the surrounding woodland.
Many aspects of California oak woodland ecology are now understood much better than they were a decade or more ago, but too little has been done to integrate this information into the management of oak woodlands. Human activities in the past one to two hundred years have altered our oak woodland ecosystems, leading to a collapse of regeneration in many parts of the state. Recent epidemics of oak mortality are the outcome of both past disturbances of the ecosystem and continuing impacts associated with human activities. If we fail to utilize the information we have learned about oaks and their associated microorganisms and insects, the condition of our oak resources will continue to decline. Knowing is not enough; we must also do.
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