Tree Declines: Four Concepts of Causality

Decline Caused Primarily by Perennial or Continual Irritation by One Factor

The factor may be a pathogen or a component of the abiotic environment. We will consider 4 examples. The first is decline of pin oaks due to inadequate uptake of iron. The principal symptoms are chlorosis and progressive dieback. If untreated, the tree slowly declines and dies (27). This disease is caused not by a pathogen but by an environmental insufficiency.

The second example is decline of sugar maple caused primarily by uptake of deicing salt. Sugar maple along roadsides in northeastern states and in Ontario began to decline during the 1950’s and 1960’s as the use of deicing salt increased. Evidence accumulated that the salt, although not the only stress-inducing factor, was primarily responsible for the decline (10, 42). In recent years, however, we don’t hear much about salt as a cause of decline in sugar maple. One reason is that where once there were many sugar maples along the roadsides, now there are few. Those that were in position to take up large quantities of chloride and sodium ions from deicing salts are gone.

Air pollutants may also cause continual stress resulting in decline, provided that the plant is intrinsically sensitive to the pollutants. Some eastern white pines, for example, are highly sensitive to ozone and also to sulfur dioxide. If chronically exposed to these pollutants, the trees lose vigor, bear only one age class of needles, and either turn yellow or show tip burn of needles. The yellowing and decline of white pines along the Blue Ridge Parkway in Virginia has been related to their sensitivity to ozone (1).

As a final example in this category, consider decline of white ash and red/green ash in central and eastern states. Although in some localities these ash species and other trees apparently decline because of stressful environment, much damage to the ash also occurs on sites where other trees appear normal and where ash formerly grew rapidly and to large sizes. Circumstantial evidence and some experimental data support the hypothesis that a microbial pathogen is primarily responsible. Declining ash in a region extending from the Great Plains to the Atlantic may be found infected by mycoplasmalike organisms (MLOs). These are submicroscopic prokaryotic organisms, lacking cell walls, that infect the phloem of trees systemically and are transmitted by certain leafhoppers and other insects that feed by sucking ploem sap. Some ash trees tolerate MLO infection for many years, but others decline and die. Matteoni and Sinclair (23) have coined the name ash yellows for the mycoplasmal disease that debilitates ash trees.

For each of the examples just cited, although one factor is primarily responsible for decline, additional factors undoubtedly contribute. Some pin oaks are genetically predisposed to damage from iron deficiency (3), and this disorder is most significant where the trees grow in neutral to alkaline soils in which iron is bound in insoluble forms (27). Salt stress causes nutrient imbalances and impairs the winter hardiness of woody plants (39). Plants weakened by air pollutant injury become abnormally susceptible to opportunistic fungi and insects that cause further damage (16, 17). Plants infected with MLOs do not become normally cold hardy, and they may sustain severe winter damage, such as split bark at the base of the trunk. Also, opportunistic fungi cause cankers and dieback in ash trees weakened by MLOs (23).

Decline Caused by Drastic Injury Plus Secondary Stress

This scheme was proposed and verified by plant pathologists and entomologists studying the role of defoliating insects in tree declines. David Houston and Philip Wargo of the U.S. Forest Service have made significant contributions to our understanding of declines that fit this conceptual scheme (11–14, 41). Consider, for example, the decline of oaks after defoliation by insects. In central and eastern states, oaks in both wild and urban forests are defoliated during sporadic outbreaks of oak leaf rollers, cankerworms, or the gypsy moth. Severe defoliation— the removal of three fourths or more of the foliar surface—may cause dieback and death, or it may predispose trees to decline caused by other agents. Defoliation is most damaging if the foliage is removed just as leaves become fully expanded. This loss triggers a second flush of growth during the same season, and the replacement growth depletes the stored carbohydrate reserves of the tree and leaves it abnormally susceptible to attack by secondary insects and opportunistic fungal pathogens. If the tree is defoliated in two successive years, food reserves are reduced to essentially nil, branch dieback begins, and water sprouts develop along the trunk and major limbs. The opportunistic organisms that most often cause further damage to defoliated oaks are rootrotting fungi, especially Armillaria species, and secondary insects, particularly Agrilus bilineatus,the two-lined chestnut borer. Larvae of this insect tunnel in the cambial region of weakened trees and girdle and kill limbs or entire trees (12, 14, 41).

Decline of street trees following construction damage to roots is another example that is best explained by a concept of two-stage causation. The massive removal of roots leads to water stress and to invasion of the wounds by opportunistic fungi, such as Ganoderma lucidum, that cause root decay. The limbs and trunks of such trees become abnormally susceptible to secondary insects and to fungi that cause cankers and decay of sapwood. By the time symptoms of decline become noticeable, the original root damage may have been forgotten.

Interchangeable Predisposing, Inciting, and Contributing Factors

In 1965-1967, Sinclair (34, 35) proposed a scheme in which multiple factors acting interchangeably may first weaken a tree, then trigger decline, and finally exacerbate the problem by their continual influence. He referred to these interacting causes as predisposing, inciting and contributing factors. The key thought in this scheme was that the introduction of a new biotic or abiotic factor or a change in the supply of a factor in an already stressful environment may trigger decline.

Manion refined Sinclair's concept in the textbook, Tree Disease Concepts (21). Manion proposed that we think of decline as a spiral of diminishing health. The tree is first predisposed by adverse factors, and its health and vigor diminish somewhat. Then another factor incites decline, and in due course various contributing factors perpetuate decline until, at the center of the spiral, the tree dies.

The concept of predisposing, inciting and contributing factors is applicable to decline of sugar maple trees in forests and sugarbushes (maple stands managed for syrup and sugar production), since multiple factors usually seem to be involved. Sugar maple grows best on moist well-drained soils where its root zone is shaded and remains undisturbed. In forests and sugarbushes, trees of this species may be weakened (thus predisposed to decline) by any of the following alone or in combination: grazing livestock, overzealous tapping and sap extraction, timber harvesting, possibly acidic deposition, and certainly defoliation by insects. If these factors stress the tree over several years, its growth will slow, and it may lose the capacity to respond to favorable factors. That is, it may begin to decline. Timber harvesting promotes decline in the residual stand because tree trunks and roots are subject to wounding during logging and to abnormal heating and drying by sunlight thereafter. These changes not only increase the possibility of drought stress, but alter the interactions of organisms in the root zone. Grazing cattle cause or contribute to decline because their hoofs break feeder roots. Sap harvesting may promote decline if too many tap wounds are made or chemicals are used that thwart compartmentalization of tap holes (causing death of a large volume of sapwood) (32) or too much sap is extracted (depleting sugar that would be used as the energy source for growth). Acidic deposition possibly also plays a role, but direct evidence for this is scant. Opportunistic organisms, especially fungal pathogens, however, always contribute to the damage. Armillaria species kill roots, and fungi such as Cerrena unicolor; Valsa ambiens, and Steganosporium species kill twigs and branches of weakened trees. These organisms are often the immediate causes of dieback (8, 12).

All maple species that are commonly planted in landscapes are also subject to decline for which the concept of predisposing, inciting, and contributing factors seems applicable. Common predisposing and inciting factors include girdling roots, restricted rooting space leading to water stress, cankers and collar rots caused by fungi (especially Phytophthora species), soil compaction leading to water shortage and rootlet mortality, deicing salt, chronic effects of Verticillium dahliae, severe trunk wounds, and root cutting during excavation. The same opportunistic fungal pathogens found in forests contribute to decline of maples in urban plantings, and they are joined there by such fungi as Ganoderma lucidum, which causes root rot, and Nectrla cinnabarina and Botryosphaeria obtusa which cause cankers and dieback (36).

As a further example, consider birch dieback. This disorder caused great damage to paper and yellow birches in the forests of eastern Canada in the 1930s to early 1950s and then subsided. Birch dieback was never fully explained (5), but both circumstantial and some experimental evidence pointed to the involvement of a climatic warming trend that occurred between 1920 and 1950 (7). Mean annual temperatures at various places in the Maritime provinces rose between 1.0 and 1.4°C during that period. It was tempting to explain birch dieback as simply a response to long-term climatic change, but this explanation was not intellectually satisfying because it did not account for the sudden onset of the dieback syndrome in a given tree (5), and it did not take into account the possible involvement of pathogens. Moreover, the magnitude of the temperature increase was insufficient to cause visible damage under experimental conditions.

Scientists studying birch dieback in Quebec and the Maritime provinces implicated heat, rootinfecting fungi, viruses, and secondary insects in the decline. For example, when the soil temperature in the rooting zone of birch seedlings was raised 2° C throughout a growing season by means of heating cables installed underneath, rootlet mortality rose from 6% in control seedlings to near 60% in the treated ones. It appeared that the altered root environment was unfavorable for mycorrhizal fungi but conducive to damage by root infecting fungi that would normally be innocuous (29). In Quebec, birch dieback was most severe where birch was most shallowly rooted. Significant damage to roots was thought to occur during open winters when roots in exposed soil were subject to abnormal freezing and drying (28). This damage would be most likely to occur during abnormally warm winters when the insulating blanket of snow is temporarily absent. As for contributing factors, the bronze birch borer (Agrilus anxius) attacked the weakened trees and in many cases was directly responsible for dieback and death. This same insect attacks and kills stressed birches In landscapes. Assorted viruslike symptoms were part of the dieback syndrome, and a strain of apple mosaic virus was eventually found in birch (6), but this virus probably had at most a contributory causal role. It was found in a much larger region than that where birch dieback occurred. Thus the concept of predisposing, inciting, and contributing factors conveniently integrates what is known about the causes of birch dieback.

Synchronous cohort senescence

The fourth concept, which I regard as a variation of the third, was elaborated by Mueller-Dombois and coworkers during the early 1980s, first as an explanation for the decline of ohia (Metrosideros coIlina) trees in Hawaiian forests (25), and later as a general explanation for assorted decline problems in North American Forests (26). The key thought in this concept is that trees of similar age, growing together, display group behaviour. As they become older and larger, they are increasingly likely to come under stress, especially as the result of seasonal water shortage. Thus they naturally become predisposed to damage that could incite decline. When a new adverse factor such as drought or a climatic warming trend causes increased stress, the trees may senesce and decline together. This phenomenon is called synchronous cohort senescence. Contributing factors, such as opportunistic fungi and insects, then hasten the decline. Mueller-Dombois et al. (26) adopted a narrow concept of disease in their discussions of synchronous cohort senescence, but neither this shortcoming nor the dissenting opinions of forest pathologists about the cause of ohia decline (9) diminishes the intellectual attractiveness of the central idea in the cohortsenescence concept.

Mueller-Dombois et al. (26) cited birch dieback and pole blight of western white pine as widescale declines for which their concept is appropriate. Pole blight, like birch dieback, was among the several tree declines that came to prominence during the 1930s and then subsided in the 1950s. Pole blight occurred, and still occurs in some localities, in scattered parts of the intermountain region of the northwestern United States and adjacent British Columbia. The name pole blight indicates that this disorder affects dominant and codominant trees that have grown to pole size (15-30 cm diameter). The symptoms include death of rootlets, slow trunk and twig growth, tufted foliage at branch tips, resinous cankers on the lower parts of the trunk, dieback, and death. The cankers are caused by opportunistic fungi, such as Ophiostoma trinacriforme,that are innocuous to trees of normal vigor. Pole blight was eventually explained as primarily a response to a temporary climatic trend of increasing temperature and diminishing rainfall (18). Young white pines growing in soils of low water holding capacity could develop vigorously during periods of normal rainfall, but during prolonged dry periods, the roots could not supply the transpirational demands of the tops, and decline resulted (19). The trees declined synchronously in groups of similar age because the members of a group were all subject to a similar level of stress. Thus the concept of synchronous cohort senescence seems highly applicable to pole blight.