Declines

Introduction

A decline disease has the following characteristics (Manion 1991):

1. a usually slow, progressive deterioration in health and vigor
2. primarily affects a mature cohort of trees
3. decreased growth and increased twig and branch dieback (applies more to hardwoods than to conifers)
4. the etiology is complex and may involve important contributions from abiotic and biotic factors.

Two controversial questions surround this topic: 1) What is a decline and how does it differ from other types of diseases? 2) What are the causal factors or etiology of some of the prominent declines, where air pollution is thought by some to play a role? The topic will be divided that way, first considering concepts of decline diseases and then examples.

Concepts of Decline Diseases

It is important to realize that we are talking here about concepts, not facts, and not even testable hypotheses. This is a topic where facts often seem to be secondary and opinions play a large role. I don't like to spend a lot time on this sort of thing because its a matter of personal opinion and preference. There is really no point in arguing about it, but we love to argue about it anyway.

Let me preface this explanation by giving credit where credit is due. Paul Manion, at the College of Environmental Science and Forestry in Syracuse, published a concept of tree declines in his textbook (Tree Disease Concepts) and in other venues. His is certainly the most cited concept of tree declines. When I was at Syracuse, I would often argue with Paul Manion about his concept. My position was that these are no different in concept and principle from any other disease or combination of diseases, and need not be separated out as a different type of disease altogether. Dr. Manion is an original thinker with strongly held opinions.

Though I enjoyed arguing with him, over the years I have become more accepting of his ideas in this matter, and have even started using it myself. This is because the concept of declines has become firmly entrenched in the practice of forest health, it is useful in organizing and conceptualizing complex causes, and because the term is widely misused and abused, so that Manion's concept is useful in restoring order to terminology and ideas. The concept presented here is essentially his, though I take responsibility for any errors.

The characteristics of declines need some discussion.

1. Speed. The term "decline" itself implies a slow, progressive decrease. In general, at least several years elapse between the first onset of symptoms and death. More often it is 10-15 years or so.
2. Mature cohort. The fact that declines affect a mature cohort in a population is an important feature that is often overlooked. Decline diseases affect trees that place the greatest demand on a site, the dominant and codominant trees. When environmental conditions are favorable, fast growth and large size are advantageous. There is a selection against small size and slow growth. But when environmental conditions are more limiting, the larger, faster growing trees are hurt most and are selected against. This is what we see as decline. This is tied into the causes of declines (see next paragraph). Mature trees place greater demands on a site than other trees and are thus more apt to suffer from unsuitable site and climatic factors, which may in turn lead to susceptibility to secondary pathogens and insects.
3. Symptoms. A key point is that these are nonspecific, very general symptoms. They are certainly not diagnostic. Dieback is usually more pronounced in hardwoods than in conifers, but branch dieback is not unusual in conifers.
4. Cause. This is the most difficult aspect of declines, both philosophically and technically. Manion's concept is most highly developed in its discussion of etiology. According to Manion (with apologies for boiling down), decline diseases are caused by interaction of abiotic and biotic factors in three groups:
1. Predisposing factors: Long-term. Often climate, site, age, genetic predisposition. May not lead to obvious problems, but predispose trees to:
2. Inciting factors: Short-term. Things like defoliation, frost damage, drought. If not for the predisposing factors, trees would recover quickly, but predisposed tree go into decline and are vulnerable to:
3. Contributing factors: Opportunistic fungi and insects like bark beetles, Armillaria root rot. These things administer the coup de grace. They finish off the tree, but normally wouldn't do so unless the tree was declining.

Seldom are declines so well understood that we can confidently identify three such agents or conditions and clearly understand their causal roles. It is particularly difficult to reliably demonstrate the role of predisposing factors. When cause is difficult to determine, it is best to simply define the phenomenon without including cause in the definition. We understand nonetheless that causes of declines tend to be complex.

Some declines are basically historic events that happened in a certain time frame. They are usually associated with episodes of drought or other climatic abnormality that serves as an inciting factor, but the time element could also be related to forest maturation in some cases.

Not everyone likes to use the decline concept. Many feel that the disease triangle is a robust model. You can think about drought weakening mature trees and making them susceptible to opportunistic pathogens as a regular old disease, without requiring a special decline model or considering it to be a special type of disease. All diseases require a particular combination of host condition, history, pathogen, and envrironment.

What is NOT a decline?

The term decline is inappropriate when used in the following cases:

1. The etiology is unknown. Of course it is handy to have a term for a syndrome or episode of mortality that is observed in a region, but it is far better to use a term that describes the actual observations. Call it mortality, or dieback, or defoliation, but don't give it a name that pretends we know what it is. To give it a disease name can create significant problems. First and foremost, it implies that the cause of the syndrome is the same wherever the term is applied. Mortality from a number of different causes may be lumped together and the cause assumed to be the same, which clearly will impede understanding of the problems. Second, it is misuse of terminology. When someone hears the term decline, they expect it to have certain characteristics, and communication is confused when we misuse terms in this way.
2. The trees die rapidly. While one may think that the forest is declining slowly over time because the trees are dying (rapidly), that is not a decline. Population and ecosystem considerations are important, but we are not talking about diseases of forests, we are talking about diseases of trees in the forest, and to think otherwise is sloppy thinking. Sudden aspen decline is apparently an exception, perhaps because aspen may die faster than most tree species. There may be other exceptions.
3. Young and old trees are affected.
4. There is more than one organism involved, such as a fungus and an insect, but the other characteristics of decline are not present. There are many associations of insects and fungi that do not cause declines.
5. Many other things that are called declines, such as global loss of forest cover through deforestation (pdf from the Center for International Forestry Research).

Here is an example of a situation where use of the "d" word may have slowed our understanding of distinct phenomena. There are several areas where oaks have declined off and on over the years. Overall, they tend to be called oak decline. In the South, a "decline" of live oak now appears to be simply oak wilt. Apparently the disease is slow and acts differently in the South.

Example - Alaska Yellow-Cedar Decline

Alaska yellow-cedar, Xanthocyparis (Cupressus, Callitropsis) nootkatensis, grows from northern California up to Prince William Sound. It is most abundant along the coast of British Columbia and southeast Alaska. In southeast Alaska and adjacent British Columbia, large areas of dead and dying yellow-cedar forests are a common sight.

This work, by a diverse team of collaborators organized by Paul Hennon in Juneau, Alaska, is the most significant work from Forest Service research during my career that I know of, and certainly in the realm of forest pathology. The problem was extremely difficult and recalcitrant. For many years, beginning in the 1980s, researchers wrestled with the problem, but there were few positive results until recently. The negative early results did serve to rule out various hypotheses, largely focusing on diseases and insects, and thus narrowed the realm of possibilities by a process of elimination. Dr. Hennon and colleagues began making careful observations of site and climate factors, developed a tantalizing hypothesis, and began to study and test the hypothesis from all angles. Although hypothesis testing goes on, there is now a high degree of confidence in the hypothesis. The work is remarkably thorough, complete, and elegant.

Here are some relevant findings of the research (Hennon et al. 2006):

1. Decline occurs in and around patches of saturated soil, or areas with soil that remains saturated for long periods.
2. Decline occurs at low elevations: greatest below 150 m and very little above 300 m.
3. Decline coincides with areas of warm winter temperatures and low snow accumulation.
4. South and west aspects (slope directions) have above average levels of decline.
5. Mortality began around 1880-1900, and has increased since about 1970.

These and many other observations and studies led to the following interpretation:

Predisposing factors

A number of factors lead to wet soils in some sites. A cooler, wetter climate beginning about 5,000 yr ago led to luxurious development of moss, which has accumulated as up to 2 m of peat. Peat absorbs large quantities of water, so peat soils are generally saturated and anaerobic. On particular sites, slope, hydrologic area and poor soil drainage also contribute to wet soils. Because the wet soils have inadequate O₂ for good root development, rooting is restricted to the soil surface. If the soil surface becomes very cold while roots are active, roots can be injured.

Because trees do not grow well on such saturated soil, stands tend to be open (D'Amore & Hennon 2006). After decline has killed trees, stands are even more open. On warm days, open stands allow more rapid snowmelt. On cold nights when there is no blanket of snow, soils are exposed and prone to freezing in open stands (D'Amore & Hennon 2006). Other site factors associated with low snowpack in late winter, such as low elevation, could also be considered predisposing factors.

Inciting factors

A Medieval Warm Period ended with the Little Ice Age, extending from roughly 1500 until significant warming in the late 1800s. Evidence suggests that yellow-cedar flourished during the Little Ice Age, when glaciers advanced farther than at any time in the last 10,000 years. Decline began with the warming at the end of the 19^th century. The climate of southeast Alaska warmed even more rapidly in the last 40 years. These warming conditions are associated with:

• Reduced snowpack, meaning less insulation for roots near the soil surface, and
• Warm late winters, which:
  • melts the snowpack earlier, and
  • dehardens (reduces the ability to tolerate freezing) yellow-cedar earlier (Schaberg et al. 2005).

However, climatic data also show the persistence of freezing events in early spring.

So on wet sites, roots are near the surface, insulating snowpack is less and melts earlier, warm temperatures render the roots more vulnerable, and canopy openings allow frost to penetrate the soil. The cumulative damage to roots weakens the trees greatly.

Contributing factors

Contributing factors are relatively unimportant in yellow-cedar decline. The preceding factors can and often do result in tree death with no apparent biotic contributor. However, two agents that are often seen associated with dying yellow-cedar and may sometimes speed mortality are Armillaria root disease and the small bark beetle Phloeosinus cupressi.

Example - Pole Blight of Western White Pine

This is a relatively simple, well understood example of a decline disease. It is really a historic problem, though it could happen again. It is explained in Manion (1991). Decline and mortality of western white pine were observed in the Inland Empire around the 1930s and 1940s.

Predisposing factors

Sites with droughty soils (soils that are shallow or have low moisture-holding capacity) were predisposed to pole blight, unless there was a subsurface source of moisture (Leaphart 1958, Leaphart & Stage 1971). Generally, root deterioration and loss of absorbing feeder rootlets developed along with or slightly preceded crown symptoms. In severely diseased trees, much of the root system was almost devoid of rootlets. Among healthy stands, those on poor soils had greater root deterioration and feeder rootlet mortality than those on good soils.

Inciting factors

A warm drought from about 1916-1940 apparently initiated the damage. Leaphart & Stage (1971) presented an astonishingly sophisticated, detailed, quantitative analysis of tree growth and its relationship to climate and occurrence of the disease. Superimposed on the sites with characteristics that predispose trees to moisture stress, successive years of moisture stress damaged root systems, reduced growth, and ultimately led to mortality.

Contributing factors

A Leptographium sp. caused a blue stain of wood and cankers on the stems and roots of affected trees (Leaphart 1956). Some isolates were strongly parasitic in some tests. Armillaria root disease was also associated with dying trees.

Conclusions

Another way of looking at pole blight is that there was a drought, and trees on droughty soils were more severely affected. They were stressed to the point that eventually they were killed by various pathogens that otherwise may not have done so. One might just call it drought damage and mortality and ignore the decline concept. In fact, the only reason it was given the disease name "pole blight" was because at first noone knew what caused it.

Although the nonnative disease, white pine blister rust, has dealt a far more serious blow to western white pine than pole blight did, there continues to be hope of introducing resistance and recovery from blister rust. Thus, the question considered at the end of the pole blight era, its likelihood of recurrence, may still be relevant. Pole blight was considered an historical oddity and was not expected to recur for many centuries under the recent historical climate regime. However, Leaphart & Stage (1971) considered another possibility that may prove to be disturbingly prophetic (citations deleted):

“Conversely, a continuing adverse climatic pattern would drastically increase the predicted probabilities of pole blight occurrence, since clusters of dry years would be both more frequent and more severe. Evidence of even warmer and drier periods than ours of 1916–1940 is recorded from studies of glaciation, of sea levels, and of vegetational successions. As experienced in the British Isles, these periods drastically affected agricultural activities, and one lasting about 200 years occurred around 1100 A.D., a relatively recent event. Although our tree-ring record and a similar though longer one of Keen's show no such long periods, such events could nevertheless be meaningful in terms of the long life of most forest trees. Lamb aptly states, ‘A table of statistics can never be substituted for a forecast’ . . .”

Example - Waldsterben and Red Spruce Decline

This one is controversial and more difficult to describe. In the late '70's and early '80's, Germans began to notice various symptoms in trees around West Germany, especially on Norway spruce. Soon, scientists were describing evidence of decline from most of the major tree species in widespread areas of Germany.

The term Waldsterben (forest death or dying) was applied to the problem, and it was characterized as a wide-ranging progressive forest decline, including many tree species, and was caused by various factors, most prominent of which was air pollution. It was predicted that it would lead to widespread devastation. A lot of money went into study of it and regular surveys were established to monitor its progress. One of the chief hypotheses was that acid rain leached nutrients from the soil and made aluminum more soluble and therefore toxic.

Then people started taking a closer look at forests in the northeastern United States. There were tree-ring studies from throughout the Northeast that purportedly showed growth decline. In spruce-fir forests, especially at high elevations, a lot of mortality was observed. Several scientists raised the alarm, talked to the media, stated that there was a widespread and serious decline and that region-wide air pollution appeared to be responsible. It was generally called spruce decline or just forest decline. There was similar concern about sugar maple, and it was called maple decline. A big research program was set up.

Now the situation is different. All along there were some that thought the evidence was insufficient, either for the existence of the declines or for a cause by air pollutants. They waited for more evidence for a while. Over time they have become more vocal in denouncing the evidence.

Growth analyses from increment cores are very complex. The data available are interpreted differently by different people. Some claim there has been a growth decline in recent decades, some say that is an artifact or that there are natural explanations for it.

Other factors have been identified. The balsam wooly adelgid, the spruce bark beetle, chronic wind stress, winter injury, and root diseases, and mistletoe have been identified as playing major roles in forests that were identified as declining.

In Germany, recent surveys have shown improvement in forest health and tree growth. There are many cases known where trees listed as symptomatic of decline had relatively obvious problems like root disease (I saw one myself). Many claim good general health for northeastern forests also.

The latest trend of interest in the Northeast is in terms of winter injury. There is almost a consensus that it may be an important factor in spruce health. But some are claiming that acidity and or ozone decrease the cold hardiness of spruce. The evidence is still equivocal.

Sometimes people mix up evidence regarding effects of acid deposition on aquatic and forest systems. Many lakes have become acidified, perhaps through acidic pollutants, and that acidification has clearly impacted the aquatic biota. But no such evidence exists for forests.

Here are some conclusions from some studies and reviews.

The people that wrote these statements are all scientists, they all had more or less the same data available for drawing conclusions. This sort of disagreement is common in science, but a lot of nonscientists don't realize it because usually the point is not of interest to anyone but those arguing. In this case it is very important and the controversy is very public.

How should you reach conclusions? Should you believe what your teacher tells you? Should you believe what you want to believe based on your biases and preconceptions? No and no. If a question is important to you, and there is reason to believe that there is controversy or the data are subject to interpretation, I hope that you will look at the data yourself. Find out how the studies were done. Be critical. That's what makes it interesting. Don't believe anything on these controversies until you've seen evidence that convinces you. As a side benefit, you will learn a lot more than if you just accept someone else's conclusions.

Warning

The use of the term "decline" has several hazards that should be fully appreciated before employing it:

• It is often a mask for ignorance of diseases and their causes.
• It may (and often does) lump a number of unrelated problems under one name, making it much more difficult to understand the causes.
• The meaning of the term is so confused and abused as to make it somewhat useless if we don't all get on the same page.
• The good old definition of disease and the disease triangle are robust enough to accomodate many diseases that we are tempted to label declines. Remember, a disease is not a pathogen! It includes consideration of host condition and environment as well.

Ha, ha, ha!!

Links