Aleppo pine blight (APB) has baffled tree experts in Arizona for decades. During our recent 2002-03 winter season the outbreak of APB was one of the worst in memory, with large percentages of mature trees showing signs of the disease in the Phoenix and Tucson metropolitan areas. “Aleppo pine disease” was first described by Prof. Rupert B. Streets in his book Diseases of the Cultivated Plants of the Southwest (1969, University of Arizona Press, p. 238). Beginning in late November, the needles on mature Aleppo pines (Pinus halepensis) suddenly die and turn brown on large sections of branches (Figure 1). As spring approaches the blight spreads to adjoining branches and is most severe in March and April. The blight will usually affect 5-40% of the limbs in a tree. However, in severe cases the blight can involve the entire crown, causing all its needles to turn brown. The whole tree appears to be dead, but close inspection reveals that most of the branches are flexible and still alive. This feature of dead needles clinging to viable, green stems is typical of APB. By May, blighted needles gradually shed and new needles emerge from denuded branches, giving the impression that the blight has vanished. However, the disorder often reappears the following winter affecting the same branches as before. Disfigurement of branch tips can occur when blighted branches dry out (Figure 2).
Plantings of Aleppo pine date back to the late 1800’s when they were widely used by the early settlers and they are mentioned in the Bible as Aleppo, Jerusalem and Mediterranean pine. They occur naturally in Mediterranean forests from Portugal and North Africa to Lebanon, Syria and Israel and they grow at elevations from 1000 to 3000 feet. Since antiquity they were known as the best-adapted and fastest growing pines for uninhabitable and abused desert sites. Their wood isn’t particularly valuable but their resin is. Ancient stone carvings from Syria verify its historical importance (Figure 5) and Greek temples were not considered complete if Aleppo pines were not planted nearby. Legend has it that the Greek god Attis severed his own genitals near a temple and they gave rise to the first Aleppo pine! The Greeks were also known to decorate Aleppo pines each year with flowers and ribbons in memory of Attis and later in honor of Jesus Christ. Europeans eventually continued this tradition, suggesting that Aleppos were the first Christmas trees.
Aleppo pines are the most popular pines for warm desert landscapes of the southwestern U.S. In Arizona they are highly valued for being extremely heat and drought tolerant and being one of the largest shade trees available for our urban desert areas. Only Eucalyptus camaldulensis rivals them in size. If one scans our skyline it becomes obvious that Aleppo pine is the most abundant, tall tree in Phoenix. The estimated appraisal value of a single 80-foot tall Aleppo pine with a 4-foot trunk diameter is well over $20,000 and thousands of such trees exist. In Phoenix alone they have a combined value of dozens of millions of dollars. That is why finding a treatment for APB is so vital.
However, the cause of APB has been never been identified so finding a cure has been difficult. Many researchers presumed that it was caused by a fungus. However, extensive study by Streets and others failed to establish a link between APB and any fungal pathogen. They made numerous attempts to isolate pathogenic fungi from sick Aleppo pines but were never successful. Streets also treated trees with fungicide, but was unable to control the disease. He concluded that a fungus was not responsible for APB and that it was caused by “environmental stress.” His recommendation for treatment was… “A mulch of manure, two or three months before the usual time of appearance of the disease, in most cases has been effective and the foliage is also a darker green.” (Ibid) However, this has not cured the disease.
The environmental stress explanation for APB is unsatisfactory for a number of reasons. For one, APB is most severe in our desert climate in winter, when our environmental stress is lowest. Also, the visual symptoms of APB do not match those of other stress-related disorders observed in trees. For example, disorders caused by heat, wind, cold, drought, high salts or nutrient deficiencies yield recognizable patterns in leaves that are uniformly distributed within a tree’s foliar crown. They often provide directional cues that point to the origin of the stress. Heat stress is usually observed on branches with south or southwestern exposure; water stress causes stunting of the entire crown; and wind stress is observed on the lee side of the tree. In contrast, branches afflicted with APB are randomly and haphazardly distributed in a tree crown. Also, in a stand of trees, APB will often strike one tree and bypass others, unlike an environmental problem such as lack of water, which affects all trees in a stand equally. One other odd feature of APB is that a tree can show blight symptoms one year and appear to recover the next, only to relapse several years later. When it reappears it tends to affect the same limbs. Taken together, these features rule against APB being caused by environmental stress such as heat or drought.
In January 2002, I attended a seminar where a renowned tree scientist from the Bartlett Tree Research Laboratory in Charlotte, NC stated that a fungus, Diplodia pinea, was the cause of APB. This contradicted the “environmental stress” explanation promoted for years in Arizona and it contradicted Prof. Streets notion that a fungus was not responsible. This researcher was not aware of Dr. Streets’ work, but he was quite certain that APB was caused by the same fungus that causes Diplodia shoot blight and Sphaeropsis blight infecting pines in the eastern U.S. Indeed, images of Diplodia-diseased trees do resemble APB (Figure 3).
One key to verifying Diplodia are the black pycnidia that arise on the needles, stems and cones of host trees (Figure 4). These fruiting bodies are easy to recognize and should also be present on Aleppo pines if Diplodia causes APB. However, why had Dr. Streets never observed pycnidia in all his years of study? I was anxious to confirm whether diseased Aleppos possessed pycnidia and I also wanted to culture Dipodia from sick pine tissue to identify the fungus.
Back at the lab I prepared a liter of sterile potato dextrose agar to culture Diplodia from sickened trees. As I looked under the dissecting microscope and selected chlorotic needles for culture, I was surprised that pycnidia were absent from all the tissues I examined. I did occasionally see a few mites crawling across the needles, but never any pycnidia. As I scanned more needles it became obvious that pycnidia were not present on any of the blighted trees. Moreover, none of my fungal cultures later proved to have Diplodia present. However, as I looked repeatedly at my samples the one consistent observation was that mites were always present on needles of blighted trees but were not present on normal trees. Could there be a link? Could these mites be the real culprits behind Aleppo pine blight?
Uncovering Mites – The Likely Cause of Aleppo Pine Blight
To investigate further, I collected mites from blighted trees throughout the Phoenix metropolitan area. I brought branches back to the lab and under the dissecting microscope and I used forceps to carefully peel back the papery sheaths (fascicles) at the base of chlorotic or pale green needles. There I observed the presence of small flat mites, 0.2 mm long, with yellow, orange or green bodies that had orange to yellow colored legs (Figure 6). These mites on Aleppo pines were extremely small and inconspicuous and never produced webs. This was the likely reason they were never identified as an agent responsible for APB. In severely infested trees, I found large numbers of mite adults and nymphs mostly hiding under the papery fascicles and crevices at the base of needles. In heavily infested branches, eggs were abundant, being bright orange-red and 0.13 mm in diameter. In trees with past infestations and on dead, blighted branches empty egg cases were observed in orderly rows of clear, translucent, hollow spheres that are 0.13 mm in diameter (Figure 7). I collected hundreds of mites, at all stages of development, and they were tentatively identified as Oligonychus, possibly O. milleri, by the Arizona State Agricultural Lab, Phoenix, AZ
As with most plant feeding mites, the mites associated with APB are slow-moving and are only observed on mature green and chlorotic needles, never on dead, straw-colored needles and never on young, newly emerged needles. Empty egg cases are consistently observed at the base of dead blighted needles, indicating past mite infestations. To the untrained observer, these empty egg cases resemble dried resin droplets. Unlike solid resin droplets, egg cases are hollow shells of uniform size of 0.13 mm.
When green branches taken from affected trees are placed under a reading lamp for several hours, mites can be seen venturing out from their hiding places to begin feeding when conditions are safe to possibly elude other predatory mites. Green needles exhibit small, circular yellow chlorotic spots caused by mite feeding damage (Figure 8). The blight occurs when the number of feeding sites becomes excessive and needles dehydrate. However, the desiccation does not extend back into the stem, rather, the drying stops at needle attachment so the stems remain viable. This type of damage would not occur with a blight caused by drought stress.
The visual symptoms and seasonal nature of APB outbreaks are wholly consistent with mite infestations, notably those caused by Oligonychus, which causes blights in other pine trees (Figure 8). In those cases, damage is scattered randomly in some limbs and trees and not others. Close inspection of needles reveals small concentric feeding sites. Also, the damage appears seasonally, as the mite populations rise and fall and they can vary in intensity between years. The mites are carried by wind and so are deposited on tree branches in a random, haphazard manner. In the case of O. milleri damage begins in fall and old needles are preferred over new young needles. Moreover, O. milleri does not produce webs.
The severity of the Aleppo pine blight on certain trees appears to be linked to mite populations. We have observed that trees in Phoenix that were almost entirely blighted to have huge populations of adults, nymphs and eggs on a single branch. In contrast, less severely affected trees are observed to have relatively few mites. There appears to be a strong genetic component with regard to an individual pine’s resistance to mite attack. This is consistent with the observation that in a stand some trees are devastated while neighboring trees go unaffected.
Subsequent to our findings a letter appeared in the April 2003 issue of Southwest Trees & Turf from J. Harold Mitchell, of Mitchell Pest Control in San Gabriel, CA about the similarity of the symptoms of Aleppo pine blight to the Oligonychus –caused problem he was familiar with in Southern California. All of the symptoms and characteristics matched with those observed for APB in Arizona. I spoke to Mr. Mitchell and we compared notes. Everything matched up. What was most ironic was that these mites were described and identified by Richard J. McCrea on Aleppo pines in Los Angeles. He used a book entitled Spider Mites of the Southwestern United States by D. M. Tuttle and E. W. Baker, which described the mite in detail. This book was published in Tucson at the University of Arizona, the same place Dr. Street worked for decades. For some odd reason the apparent real cause of Aleppo Pine blight was never uncovered in Arizona where it was first discovered. That is the real mystery.
