UNIVERSITY OF CALIFORNIA COLLEGE OF AGRICULTURE AGRICULTURAL EXPERIMENT STATION BERKELEY 4, CALIFORNIA CONTROLLING ARMILLARIA ROOT ROT IN CITRUS DONALD E. BLISS' Certain practical suggestions can be made toward controlling arraillaria root rot, which is causing widespread concern among citrus growers in southern California. This disease is caused by a toadstool-forming fungus known as the oak root fungus or as Armillaria mellea (Vahl) Quel. Armillaria is native to California on oaks and other woody plants. It is now found on many wild and cultivated species, including some of great economic importance. Armillaria root rot spreads from place to place on infected wood. This wood may be a root fragment, or part of an infected nursery tree; it may be carried by flood water or by a delivery was originally brought under cultivation. In this way armillaria has had an opportunity to be- come widely distributed. Citrus, though con- siderably more resistant to armillaria root rot than the stone fruits, has already suffered se- verely; and the losses are becoming even greater each year as the disease continues to spread. Recognition of the Disease In citrus, armillaria becomes well established in the roots before any visible effect appears in the top. There may be a gradual deterioration in vigor, with the foliage yellowing and dropping Fig. 1. --White, mycelial fans of Armillaria mellea between the bark and wood of an infected citrus root. The disease had been moving inward along this root toward the root crown. Its development was arrested, however, when the advanc- ing lesion entered the dry atmosphere of a pit dug earlier about the root crown. cruck. Many infested areas date back to an in- fected oak or pepper tree. Long after the aerial parts of the tree are gone, the fungus remains alive in the roots, a potential source of infec- tion to healthy trees of all ages. In some agri- cultural sections there has been a succession of susceptible tree crops, including stone fruits, walnuts, and citrus, since the time when the soil Associate Plant Pathologist in the Experiment Station. over part or all of the tree; or there may be a sudden wilting and collapse. In either case, death eventually follows. Since these symptoms resemble those of various other root troubles, the disease usually cannot be diagnosed with cer- tainty unless signs of the causal fungus are dis- covered also. A white, felty, fan-shaped growth of fungus mycelium under the bark constitutes the most re- liable sign of armillaria root rot (fig. 1). Other signs helpful in diagnosis are cordlike, [1] purplish-brown rhizomorphs on the surface of diseased roots and light-brown toadstools appear- ing occasionally aboveground in late fall (figs. 2 and 3). The rhizomorphs resemble small, dark roots except that they are smooth and shiny when fresh and are differently branched. The rhizo- morph consists of an outer brittle shell, and a Fig. 2. --Two citrus roots with rhizomorphs of Armillaria mellea . The rotted wood is soft and jellylike. Fig. 3 .--Toadstools of Armillaria mej lea at the base of a dead tree. light-colored, towlike center composed of fungus threads. Koots of the higher plants have a tough, woody core. Infection and Spread Armillaria infection is accomplished by di- rect penetration of a rhizomorph into the bark. The fungus kills the tissues as it spreads out- ward from the point of infection. It also in- vades the underlying wood, whereas the disease is confined at first to a very small, localized lesion, it may spread throughout the root, thence to other roots, and finally girdle and kill the trunk at the root crown. After becoming estab- lished, the parasite sends out new rhizomorphs. These may grow' in any direction along the surface of the root from which food is being obtained, or may extend outward into the soil for a few inches. Armillaria root rot spreads from tree to tree in citrus orchards at the rate of about one tree row every two years. Healthy roots of a diseased tree or those of neighboring trees may be at- tacked in places where they are closely associ- ated with infected roots. Apparently the fungus cannot exist permanently in soil that is devoid of woody material. Survey In detecting and controlling armillaria root rot, vigilance is of prime importance. All trees in and about a citrus orchard should be surveyed once a year for signs or symptoms. A grower should know the history of his land, and the lo- cation of former washes, creeks, and native trees--all potential avenues of infection. Dead stumps should be viewed with suspicion; also areas where the trees are sickly or have died. Windbreaks, roadside trees (especially pepper trees \ and ornamental plants in dooryards are liable to be infected. Armillaria will spread rapidly through the roots of such plants when the tops are removed. A good map will aid the grower in surveying his orchard. The map should be large enough to shoW the location of each tree. Individual blocks, rows, and trees should be numbered. The situation in regard to armillaria root rot can be indicated in detail by symbols. These may be altered as conditions change, or a new map may be drawn for each survey. Such records are valu- able for later reference. The grower can best make a survey for armil- laria root rot by walking up and down the rows , looking at each tree for symptoms. The toad- stools of armillaria appear on the most severely affected trees in late fall after the first storms of the rainy season. If the disease is suspected, one may examine the root crown by re- moving the topsoil. A tree showing distress from armillaria will usually have one or more dead roots. After locating the visibly affected trees, the outer limits of infestation should be deter- mined in preparation for certain control meas- ures. Root lesions occur before tops begin to deteriorate. All healthy-appearing trees adja- cent to infected trees should therefore be re- garded with suspicion. Their crown roots are examined, especially those on the side near the infested area, to determine whether armillaria [2] has reached the trunk. If it has not, a shallow test trench is dug midway between the two trees at right angles to a line connecting them. The condition of the roots in this trench will indi- cate roughly how far the disease has spread in that direction and also whether the healthy- appearing tree can be protected. At this early stage of the survey it is not practicable to examine all the roots between the two trees. The roots of other healthy-appearing trees about the edge of the infested area should first be inspected in a similar, preliminary manner. The object is to obtain the most in- formation with the least work. Finally, when all advance information is plotted on the map, one or more centers of in- fection may be found to exist in the orchard. A continuous trench may then be dug around each infested area. It should be as deep as the deep- est lateral roots (4 to 5 feet) and wide enough for a man to work. This trench will expose, for examination, all roots that cut across its path; it may also serve as a chemical trench barrier against further spread (.see "Prevention"). The trenched area should include all trees that are diseased or suspected. Healthy trees are some- times also included in the area because it is not practicable to exclude them. As an extra precaution, an entire row of healthy or healthy- appearing trees may be left between the trench and the infested area. The continuous trench is usually dug in the middle, halfway between the tree trunks. If it runs too close to the infestation so that diseased roots are found to cross it, the trench should be rerouted to include all the soil that contains armillaria. All earth excavated from the trench should be thrown toward the infested area to prevent possible spread. The grower, on completing a trench, must be reasonably sure that the entire root-rot area about one center of the trouble has been surrounded. The subsequent treatment of the trench and of the infested area is discussed in the following sections. Prevention Where citrus orchards are being planted, the use of healthy nursery stock in noninfested soil is perhaps the most important and most practical way to control armillaria root rot. Nursery stock is usually free from the disease, but even a single infected tree can form a center of in- fection. The problem of obtaining clean soil is more serious; an infestation may already have de- veloped from previous orchards and native trees. To plant a citrus orchard in such soil is to in- vite disaster. Means of eradicating amillaria are known (see "Eradication in Infested Soil") and should be employed before the orchard is planted. No citrus rootstocks are known to be immune or very resistant to the strains of Armillaria m ellea in southern California. Certain growers in one section of the state believe that the sour-orange rootstock is more resistant than the sweet-orange. Elsewhere, however, this belief has not been substantiated. Tree roots of all kinds seem to become more susceptible to annil- laria after the top has been removed. For this reason, it is safer to retain a living infected tree standing in or near an orchard than to cut away the top without also destroying the roots. Large oak and pepper trees create a difficult problem in this regard. The toadstools of this fungus, though probably of minor importance, should be destroyed before the spores are discharged. Another preventive measure is the control of flood water. If for no other reason, flood water should not be al- lowed to pass through an orchard because of the danger that it may carry and deposit fragments of infected wood. Trees growing on the banks of a creek or wash are liable to become infected from piles of trash in the stream bed. Willows and poplar trees, sometimes planted along streams to prevent soil erosion, are very sus- ceptible to armillaria; but palms and tamarisk ( Tamarix articulata ) are immune. To keep armillaria root rot away from the ■ healthy trees of an infected citrus orchard is usually more important than to treat the dis- eased trees. Further spread from an infested area may be prevented by total eradication (see "Eradication in Infested Soil") or by a chemical trench barrier. Physical barriers made of con- crete, galvanized iron, roofing paper, and the like, are not recommended. The chemical trench barrier is designed to maintain a root-free zone about the infested area. Since the rhizomorphs of armillaria re- main closely associated with the diseased roots from which they grow, a chemical soil treatment that will prevent roots from crossing the bar- rier will also prevent the development of rhizo- morphs and the infection of healthy roots out- side the enclosure. Starting with an open continuous trench sur- rounding an infested area (see "Survey"), a chemical trench barrier (fig. 4) is made as fol- lows : 1. Apply carbon disulfide (CS 2 ) in a single line of charges along the bottom of the trench at the rate of 2 liquid ounces every 18 inches and in holes 8 inches deep. Tamp the soil over each charge immediately, to prevent the rapid escape of fumes. 2. Fill the trench with the soil that was previously excavated from it. Compact the soil by tamping, but do not settle it with water. 3. Apply carbon disulfide in a single line of charges along the top of the filled trench at the rate of 2 liquid ounces every lb inches and in holes 8 inches deep. Tamp the soil over each charge immediately, and moisten the soil over the trench and to a distance of 2 feet on both sides, with water to a depth of 3 inches tc prevent rapid escape of the fumes. [3] 4. After the original treatment of the filled trench, at intervals of 6 months (preferably when the soil is dry) , apply carbon disulfide in a single line of charges along the chemical trench barrier at the rate of 2 liquid ounces every 18 inches and in holes 8 inches deep. Tamp and moisten the soil surface as described in paragraph 3. The line of chemical treatment should always coincide with the middle of the original trench. This line should be accurately located on the survey map previously described. /-•-WATER SEAL n preparing a chemical pen trench with a charge lied at the bottom; B, soil and treated with a ide at the surface. Top- 3 inches (the wet area each side of the trench] The B treatment must be to prevent tree roots llaria from crossing the Fig. k- --Two steps i trench barrier: A, an o of carbon disulfide app the trench filled with charge of carbon disulf soil , wet to a depth of extending out 2" feet on forms the water seal repeated every 6 months and rhizomorphs of armi filled trench. Treatment The treatment of armillaria root rot is de- signed to favor the suscept (the citrus tree) and to suppress the pathogen (armillaria). Proper treatraent in the early stages of the disease may temporarily lengthen the life and usefulness of the tree, or it may prevent death for an inde- finite period. Economic considerations will de- termine how much treatment is feasible. Since armillaria is very sensitive to drying, a pit may be dug about the root crown and left open indefinitely. The growth of the fungus is arrested by exposure to the air, especially where it is moving inward along the roots toward the trunk (fig. 1). The tree, although showing distress, will not die until most of the roots are infected or until the trunk is girdled. Surgery is most effective in the early stages of the disease because then only a small part of the root system is involved, and the loss of a few roots is not serious. A tree can be cured if all the lesions are. removed, but this is rarely practicable. Surgery is usually confined to the region of the root crown and is done in combination with the aeration treatment men- tioned above. Protection of the trunk at the root crown by preventing the fungus from reach- ing it is of vital importance. Clean cuts should be made into the noninfected wood surrounding the lesion, and the wound painted with some wound dressing. The infected wood should be destroyed. Generally speaking, armillaria appears to thrive under the same environmental conditions that favor the growth of oranges and lemons in southern California. The disease has not been reported in the hot, inland Coachella and Im- perial valleys, where the principal citrus crops are grapefruit and tangerines. Eradication in Infested Soil The destruction of armillaria in infested soil may be accomplished by disinfection with carbon disulfide (also spelled carbon bisulfide and car- bon bisulphide). Soil disinfection is best adapted for treating small areas. The cost seems considerable; but, when viewed from the stand- point of disease prevention, it is really low. Soil disinfection with carbon disulfide in- volves removal of the diseased citrus tree and fumigating the soil. All trace of the chemical disappears from the soil within 4 to 8 weeks after treatment , and another tree can then be planted. Carbon disulfide has been used against armillaria root rot in southern California for nearly thirty years and is known to be effective. The method has recently been improved, so that this chemical can now be applied by any grower. For best results the soil should be as dry as practicable. Light, permeable soils are easily fumigated; .heavy, impermeable soils are not. Setter penetration can be expected in warm soils than in cold although, in southern Cali- fornia, soil disinfection is successful at all seasons. The grower should determine the ap- proximate size and location of infected roots and should provide some means for confining the disinfecting gas in the soil. The -steps to be taken in eradicating armil- laria from a citrus-tree square are as follows: 1. Pull the diseased tree with as many roots as possible. All roots more than 2 inches in diameter should be removed before the soil treat- ment begins. 2. Level the soil, smoothing the surface, and let it become as dry as possible. 3. Apply carbon disulfide (equipment is de- scribed later) over the entire area of the tree square (or to the skirts of the adjoining trees) at the rate of 2 liquid ounces per charge every 18 inches, in rows 18 inches apart (fig. 5). Stagger the charges to make a triangular or diamond-shaped pattern. Apply the charges 8 inches deep in sandy soil; 6 inches deep in heavier clay loam. 4. Apply four depth charges of carbon disul- fide about the location where the diseased tree [4] stood; the rate is 6 liquid ounces per charge, 4 feet apart and 4 to 6 feet deep (fig. 6). Use a soil tube for making the holes and for de- livering the chemical at the proper depth. 5. Tamp the soil over each charge immediately to prevent rapid escape of the fumes. 6. Moisten the soil with water over the en- tire treated area to a depth of 3 inches to con- fine the gas. This blanket of wet soil should be maintained for 3 weeks. Rake the surface if there is a tendency toward cracking. A layer of canvas or glue-coated paper may be substituted for the water seal. To confine the gas properly is very important. ROW I ROW 2 ROW 3 ROW 4 •— 18"-* CHARGES OF CARBON DISULFIDE T 00 ROW 5 oU r ROPE WITH KNOTS J3, Fig. 5 • --Suggested spacing of carbon disul- fide charges applied at the surface to eradi- cate armillaria from infested soil. A rope with knots at 18-inch intervals marks the points of application. The charges in the even-numbered rows are staggered to make the triangular or diamond- shaped pattern. 7. Allow the soil to dry, or remove the cover. 6. Replant when the odor of carbon disulfide can no longer be detected in the soil. Under favorable conditions, the vapor of car- bon disulfide from the 2-ounce charges will penetrate to a depth of 5 or 6 feet, and should kill all the armillaria in the soil and in roots up to 2 inches in diameter. The 6-ounce charges normally will eradicate the fungus in the deep- est taproots if the soil is reasonably dry and permeable. Several kinds of hand applicators for carbon disulfide have been used successfully. Recently, however, a self -measuring, force-feed type (fig. 7) has been developed that combines such desir- able features as convenience in handling, ease and speed of operation, and accuracy in dosage. With one stroke of the plunger, liquid carbon disulfide is forcefully ejected from several small holes near the point of a steel prod. The chemical is forced into the soil 3 or 4 inches in all directions from the prod, which is in- serted by means of foot pressure to the desired depth. A piece of small hemp rope and a few stakes are necessary additional equipment. The rope 's knotted at lb-inch intervals and then ^5 6 7 - 8 - 9 - 10 - CHARGES OF CARBON DISULFIDE Fig. of a lar ing the to eradi rotted t tree was the orig system. ) placed 5 laria in plied at seal pre 6. --Vertical s ge , deep-roote placement of c cate armillari aproot remaine pulled. (The inal position Heavy charge feet below th these roots. a depth of 8 vented rapid e ection through root zone d citrus tree, illustrat- arbon disulfide charges a. The lower ends of the d in the soil when the broken lines indicate of other parts of the root s of disinfectant were e surface to kill armil- Other charges were ap- inches. A 3-inch water scape of the fumes. T i Fig. 7. --Self- measuring, force-feed type of applicator for carbon disulfide. This applicator, known as "Mack's Fumi- gant Injector," is distributed by the manufacturers of car- bon disulfide. (See footnote 2. Illus- tration by courtesy of Wheeler, Reynolds, and Stauffer. ) [5] stretched across the infested area, beginning at one side. After a charge of carbon disulfide is applied to the soil beneath each knot, the rope is moved 18 inches to one side, and the position of the knots is staggered in relation to that in the first row. The third row is like the first; the fourth, like the second; and so on (fig. 5). The commercial grade of carbon disulfide 2 is a colorless, readily volatile liquid, with an unpleasant but distinctive odor. CAUTION : The liquid is inflammable; the vapor is highly explosive when mixed with three times its volume of oxygen or air and exposed to a flame, or it will explode by autoignition at 300° F. Carbon disulfide, although inf lammable , may be handled with confidence and security if one takes the same precautions as with gasoline. Some cardinal rules for handling this chemical follow: 1. Store in a cool place. When using from a container in the field during warm weather, cover it with wet burlap to prevent expansion and excessive evaporation of material. 2. Do not light matches near this chemical, nor smoke. 3. Never use a hammer and chisel to loosen a bung, because of fire hazard. Use a wrench made to fit the countersunk hole, or cover the bung with wet burlap and open with a Stillson wrench. Allow the gas pressure to become equa- lized before completely opening the bung. 4. To preclude the accumulation of static electricity, do not use glass or crockery con- tainers when drawing the liquid. Either rest the drum on the ground, or ground it by means of a chain, one end of which is buried in moist soil. 5. Do not inhale the concentrated fumes con- tinuously. Two liquid ounces (59.15 cubic centimeters or 2.5 avoirdupois ounces) of carbon disulfide, applied at 18-inch staggered intervals, will treat an area of 2.25 square feet. The volume required for treating 100 square feet is 88.9 liquid ounces (0.6945 gallon); that for an acre, 302 gallons. Carbon disulfide may be obtained in 5-, 10-, or 55-gallon lots. The cost of the chemical to treat one tree square, 20 by 24 feet, according to the present recommendation, is about $2.82 (3.53 gallons at 80 cents per gallon) Recommendations . 2 Wheeler, Reynolds, and Stauf f er , 636 Cali- fornia Street, San Francisco, are the principal manufacturers of carbon disulfide on the Pa- cific Coast. Their Anchor brand is suitable for soil disinfection. In controlling armillaria root rot, the grower is concerned with treating the trees al- ready infected and with preventing spread to the adjoining healthy trees. Since no two situations are alike, he should use judgment in selecting control measures. Methods of disease prevention and treatment should be followed wherever prac- ticable. Total eradication is recommended for small infested areas. Partial eradication (soil disinfection after the removal of worthless trees) is suggested where the infestation is widely distributed and where trenching is not practicable. A chemical trench barrier and partial eradication are recommended where many diseased trees are grouped together and where armillaria is spreading to noninfested areas (fig. 8). This combination treatment may even- tually lead to total eradication. Soil disin- fection does not preclude reinfestation, how- ever, and overlapping is necessary where con- tiguous areas are disinfected in different years. Questions concerning the identification of ArniJlaria mellea and the effectiveness of con- trol will be answered by the local farm advisors of the Agricultural Extension Service. Pertinent Literature Two useful circulars on control measures-- No. 200 and No. 204--have been issued by the Wheeler, Reynolds, and Stauf fer Company, 636 California Street, San Francisco, California. Other publications on armillaria root rot are listed below. Fawcett, H. S. 1936. Citrus diseases and their control. 2d ed. 656 p. McGraw-Hill Book Co., Inc., New York, N.Y. S. Oak root fungus control demands careful attention. Citrus Leaves 19(2): 1, 15. Thomas, Harold E. The identification and treatment of armillaria root rot. Almond Facts 613.): 3-4. LaRue , R 1939. 1942. [6] LEGEND: G o G ® o o O ® O © ® o o ® O (P) • G o ® ® o • R R • © S X R R R CO o® • w ® G ® C°) ® (o) G o R HEALTHY TREE SLIGHTLY INFECTED SEVERELY INFECTED REPLANTED TREE AREA TO BE DISINFECTED AREA PREVIOUSLY DISINFECTED CHEMICAL ' TRENCH-BARRIER Fig. 8. --Map of a citrus orchard, illustrating a method of controlling armillaria root rot, A survey trench was first dug about the infested area. The trench was then treated to form a chemical trench barrier. Severely infected trees were removed as they became commercially worthless. The soil was disinfected in a rectangular area extending to the skirts of the ad- joining trees, or in overlapping areas that had been previously disinfected. Treated areas were replanted with healthy trees. The treatment of the chemical trench barrier will be dis- continued when all the soil within the barrier has been disinfected and when no further evi- dence of infestation remains. 5m-Apr. ,'47(A3325) [7] Taor