UNIVERSITY OF CALirOBMIA PPBLICATI0N8 COLLEGE OF AGRICULTURE AGRICULTURAL EXPERIMENT STATION BERKELEY, CALIFORNIA GUM DISEASES OF CITRUS TREES IN CALIFORNIA BY HOWARD S. FAWCETT BULLETIN No. 360 April, 1923 UNIVERSITY OF CALIFORNIA PRESS BERKELEY, CALIFORNIA 1923 David P. Barrows, President of the University. EXPERIMENT STATION STAFF HEADS OF DIVISIONS Thomas Forsyth Hunt, Dean. Edward J. Wickson, Horticulture (Emeritus). , Director of Resident Instruction. C. M. Haring, Veterinary Science, Director of Agricultural Experiment Station. B. H. Crocheron, Director of Agricultural Extension. C. B. Hutchison, Plant Breeding, Director of the Branch of the College of Agriculture at Davis. H. J. Webber, Sub-tropical Horticulture, Director of Citrus Experiment Station. William A. Setchell, Botany. Mybr E. Jaffa, Nutrition. Ralph E. Smith, Plant Pathology. John W. Gilmore, Agronomy. Charles F. Shaw, Soil Technology. John W. Gregg, Landscape Gardening and Floriculture. Frederic T. Bioletti, Viticulture and Fruit Products. Warren T. Clarke, Agricultural Extension. Ernest B. Babcock, Genetics. Gordon H. True, Animal Husbandry. Walter Mulford, Forestry. James T. Barrett, Plant Pathology. W. P. Kelley, Agricultural Chemistry. H. J. QuAYLE, Entomology Elwood Mead, Rural Institutions. H. S. Reed, Plant Physiology. L. D. Batchelor, Orchard Management. W. L. Howard, Pomology. *Frank Adams, Irrigation Investigations. C. L. Roadhouse, Dairy Industry. R. L. Adams, Farm Management. W. B. Herms, Entomology and Parasitology. John E. Dougherty, Poultry Husbandry. D. R. Hoagland, Plant Nutrition. G. H. Hart, Veterinary Science. L. J. Fletcher, Agricultural Engineering. Edwin C. Voorhies, Assistant to the Dean. DIVISION OF PLANT PATHOLOGY J. T, Barrett E. T. Bartholomew II. S. Fawcett C. O. Smith * In cooperation with Division of Agricultural Engineering, Bureau of Public Roads, U. S. Department of Agriculture. GUM DISEASES OF CITRUS TREES IN CALIFORNIA* BY HOWAED S. FAWCETT CONTENTS PAGE Introduction 370 Pythiacystis (brown rot) gummosis 371 History 371 Symptoms 373 Investigations into the nature and cause of the disease 376 Resistance of different species and varieties 378 Conditions faciUtating infection and development of the disease 381 Fusarium as a secondary aid in the development of Pythiacystis gummosis.. 384 Methods of control 385 Prevention 385 Treatment 387 Mai Di Gomma or footrot 397 Symptoms 397 History 398 Investigations 398 Control 400 Botrytis gummosis 401 Symptoms and occurrence 401 Investigations as to nature and cause 402 Factors favoring the disease 402 Methods of control 404 Prevention 404 Treatm-nt 404 Sclerotinia gumming due to Sderotinia Ldbertiana 406 Psorosis (scaly bark) of orange trees 408 Symptoms 408 Investigations as to cause and manner of development 408 Experiments in treatment 410 Suggestions for treatment 413 Diplodia gumming 416 Twig gumming 417 Exanthema or dieback 418 Nature and symptoms 418 Control r. 419 Minor forms of gumming 419 Gumming due to Penicillium roseum 419 Gumming due to Fusarium sp 420 Gumming due to Alternaria sp 420 Gumming due to Bacterium citriputeale 420 Gumming associated with insect injuries 421 Gumming associated with chemical stimuli 421 Physical effects of the environment 422 Summary of directions for prevention and treatment 422 * Paper Xo. 92, University of California, Graduate School of Tropical Agriculture and Citrus Experiment Station, Riverside, California. 370 UNIVERSITY OF CALIFORNIxV EXPERIMENT STATION INTRODUCTION The aim of this bulletin is to bring together the information now at hand regarding the so-called gum diseases of citrus and the various minor forms of gumming in citrus trees under California conditions. Special emphasis is here given to contributing conditions and to methods of prevention and treatment. A considerable amount of investigational data not heretofore published is included. The results of investigations in other phases of these diseases are being published in the Journal of Agricultural Research. These latter phases will therefore receive only brief treatment here in order to avoid undue duplication. It is necessary, however, to duplicate in part the descrip- tions of the diseases and a small amount of other data. Previous investigators had come to the conclusion that all gum diseases of citrus trees in California originated independently of micro-organisms.^ It was held that these diseases were largely auto- genous in their nature, and frequently induced through the effects of certain climatic or soil conditions alone. It now appears evident that these environmental conditions cannot by themselves initiate the severe forms of gummosis in citrus earlier attributed to them, although certain factors are found to play (as they do in most para- sitic diseases) an important role as contributing conditions which favor infection and invasion of the host hy the causal parasites. The investigational work on which the greater part of this bulletin is based was begun in February, 1912, under the direction of the State Commission of Horticulture and continued after October, 1913, at the Citrus Experiment Station of the University of California. Acknowledgment of the assistance rendered during this investigation has been given elsewhere.^ The names of species and varieties of Citrus will be used in accordance with Swingle^ as follows : common lemon. Citrus limonia Osbeck; rough lemon, a horticultural variety of C. limonia Osbeck; sweet orange, C. sinensis Osbeck ; sour orange, C. grandis Osbeck ; citron, C. medica Linn.; trifoliate orange, Poncirus trifoHata Raf. The word lemon, when used alone will refer to the common lemon, and the word orange to the sweet orange. 1 Smith, It. E., and Butler, O. Gum disease of citrus trees in California. Calif. Agr. Exp. Sta. Bull. 200, pp. 235-272, 3908. 2 Fawcett, 11. S., Two fungi as casual agents in gummosis of lemon trees in California. Monthly Bull. Calif. State Comm. of Horticulture, vol. 2, pp. 601-617, 1913. 3 Swingle, W. T., "Citrus," in Bailey, L. H., Standard Cyclopedia of Horti- culture, vol. 2, pp. 270-785, New York, 1914. Bulletin 360] gUM DISEASES OF CITRUS TREES IN CALIFORNIA 371 PYTHIACYSTIS (BROWN ROT) GUMMOSIS HISTOEY A destructive form of gum disease similar to Pythiacystis gum- mosis first attracted serious attention in the Azores about 1834. A similar gum disease appeared in Italy as early as 1863 ; in Portugal, 1865 ; in Australia, 1867 ; in Spain, 1871 ; in the United States, 1865 ; and in most other citrus regions before the year 1890. See accounts and references by Savastano^ Swingle and Webber,^ Butler^ and Fawcett.'^ In the early history of citrus growing in California there appears to be no record of the occurrence of gum diseases until about 1875.^ Not long afterwards they became an important hindrance to commer- cial citrus culture, as is evidenced by the horticultural literature of the time. A committee of citrus growers appointed to examine the condition of citrus orchards, stated in 1878^ that at that time few localities were free from gum disease, which this committee believed was caused by excessive irrigation and unsuitable cultivation. The orchards most heavily flooded with irrigv.tion water, especially on heavy soils, were found worst affected. The application of manure immediately around the trees was also reported as tending to promote the disease. Lemon roots were found to be more susceptible than orange roots, and in a discussion which followed this report much objection is expressed to lemon and Chinese lemon stock as compared with sweet orange. Light soils were thought by many to be better adapted than hea\'y soils for orange culture since orchards on light soils were healthy while those on heavy soils were rapidly dying out, presumably from gum disease. Irrigation by flooding was a common practice at that time and later^*^ it was stated as a settled fact that the lemon (on lemon roots) is peculiarly sensitive to moisture and easily begins to rot if water is 4''Gommosi degli agrumi, " in Patologia arborea applicata, bp. 127-141. Napoli, 1910. 5 The principal diseases of citrus fruits in Florida. U. S. Dept. Agr. Div. Yeg. Phys. & Path. Bull. 8, pp. 1-42, 1896. 6 A Study on Gummosis of Prunus and Citrus, Ann. Bot., vol. 25, pp. 107-153, 1911. 7 Gummosis of Citrus, Jour, of Agr. Eesearch. (In press.) 8 Mills, J. W., Citrus fruit culture. Calif. Agr. Exp. Station, Bull. 13.8, pp. 1-46, 1902. 9 Southern Calif. Horticulturist, vol. 1, p. 115, Jan., 1878. 10 Southern California Horticulturist, vol. 1, pp. 314-315, July, 1878. 372 UNIVERSITY OF CALIFORNIA EXPERIMENT STATION left standing* around it. In the following year the statement was made in the same publication^^ that gum disease is induced by mid- summer irrigation and that lemon trees on their own roots were dying rapidly. In 1882 a leading nurseryman^^ regarded gum disease as the only citrus trouble of importance. Of the four citrus stocks commonly used at that time (sweet orange, lemon, lime and citron) the lemon and the lime were stated by Gary to be the most fatally affected with this disease. He advises the use of the sweet-orange stock but says nothing of the sour orange which was introduced at a later date. Gary's description of the disease and his reference to the differences in susceptibility of varieties indicate that the type of disease spoken of was Pythiacystis gummosis. Because of the susceptibility of the lemon the growers gradually dis- covered that other stocks must be used. The universal verdict accord- ing to Holt^^ in 1892 was that lemons should not be grown on their own roots. Sweet-orange stock though much less susceptible than lemon was also frequently affected with gummosis. This fact drew attention to the sour-orange stock which had been used successfully in southern Europe and in Florida to replace trees affected with mal di gomma. This resistant stock only gradually came into use as a preventive of gum disease in California. Cutter^^ in 1892 stated that his attention w^as called first to the value of the sour-orange as superior to sweet in its resistance to gum disease in 1885. The following year the firm of Twogood, Edwards and Cutter of Riverside, received the first shipment of sour-orange trees from Florida for commercial purposes ; although a few trees had been grown from Florida seeds for test by others before this time. In the light of our present knowledge of varietal susceptibility of citrus to gum diseases and of the part played by heaw soils and by excessive irrigation (especially flooding on heavy soils), the failure in growth on lemon stocks, and the dying of trees on heavy soils, but not on lighter soils Avould now appear to have been due to the presence and attack of gum disease organisms, especially Pythiacystis citropththora Smith and Smith. The early discontinuance of the use of lemon, lime and citron as stocks, and the adoption of the orange as a general stock for all 11 Southern Calif. Hort., vol. 2, pp. 83-86, March, 1879. 12 Gary, Thomas A., Orange culture in California. Pacific Rural Press, pp. 81-82, San Francisco, 1882. 1-5 Holt, L. M., "Lemon culture for profit," Proc. Calif. Pomological Soc, 1892. 14 Cutter, J. E., Proc. Calif. Pom. Soc, 1892. Bulletin 360] gUM DISEASES OF CITRUS TREES IN CALIFORNIA 373 varieties appears to have been largely brought about by this one disease. Sour-orange stocks were introduced from Florida later, as previously indicated, for the purpose of combating this disease on heavy soils, but this stock has not become of Avidespread use in Cali- fornia until recent years. SYMPTOMS Pythiacystis or brown-rot gummosis with its associated rot of the fruit^^ is probably the most widespread and destructive of the citrus gum diseases. On the lemon (the most susceptible variety) patches of bark on the trunk are kiued and often large quantities of gum are exuded (figs. 1 and 2a.) Infection usually starts at the base of the trunk or on the crown roots and works rapidly both upward and laterally. The bark is killed (not as in cases of Psorosis and shell- bark, merely in the outer cortical layers) but entirely through to the wood, thus including the cambium. A thin layer of wood tissue only about Vrz of an inch thick is visibly affected unless secondary organ- isms enter. The bark above the soil is not softened as it is in the early stages of Botrytis gummosis but remains firm and intact until drying causes it to shrink and crack longitudinally (fig. 2h). Below the surface of the soil secondary organisms frequently set up fermen- tation and moist decay. On the bark of old orange trees and other partially resistant varieties often the progress of the disease is soon arrested and the lesions tend to become self -limited. The loss of large patches of bark is followed by a gradual yellowing and dropping of leaves on the branches leading out from the portion of the trunk aifected. Although these are the main characteristics of the disease as seen on superficial examination, there are many special features which appear when more careful study is given to its development under various conditions. In the earlier stages of the disease the exuding gum is usually the only external symptom (fig. 2a). By lightly scraping the bark at this time the margin between the sound and invaded tissue is shown indefinitely, only by the gradual shading of the normal green color into a drab. The bark is not softened but remains firm and only after a considerable time does it shrink and crack longitudinally (fig. 2h). On healthy, rapidly growing lemon trees the area of killed and darkened bark, which is elliptical or irregular in outline, is usually 5 to 10 inches in vertical length and half that in width, when the gum 15 Smith, R. E. and others, The Brown Eot of the Lemon. Calif. Agr. Exp. Sta. Bull. 190, 70 pages, 1907. 374 UNIVERSITY OF CALIFORNIA — EXPERIMENT STATION first becomes apparent. By that time the fungus has invaded the the bark at this time will show that the outer margin of the invaded zone in the inner tissues is about coextensive with that seen on the surface. The upward and downward extension from the point of infection is usually many times greater than the lateral extension. In an irregular zone or band surrounding an actively invaded area, the cambium layer shows an influence extending from the margins of the dead bark. There is a production of clear, watery gum which seems to originate in the region of the embryonic wood among the live cells without any apparent fermentation or decay. This region, not yet darkened, outside the invaded portion, will be spoken of in this paper as the ''outer gummous zone" (fig. 3h). It may in time extend considerable distances upward and downward and small distances laterally from the margin of the invaded zone (fig. 3&). It has been traced for 2 and 3 feet upward. The extent of this outer gummous zone varies with the age and rapidity of development of the disease lesion, the condition of the tree, etc. The inner surface of the bark in the invaded zone in a lesion of considerable size varies in color from mineral brown to burnt amber or fawn^^ and the same discolorations will be found on the surface of the wood just at or beneath the cambium (fig. Sh). The discoloration does not extend far (usually only %2 to % of an inch) into the woody layers. The cambium region in the gummous zone is chamois to yellow ochre in color, gradually fading at the margins into the normal color of the sound woody surface. Frequently, when the bark is irregular in contour, gum pockets 1 to 2 inches in length will be formed. The gum accumulates near the cambium and by pressure separates the bark from the wood at certain places, forming definite pockets. The pressure is usually relieved by a break in the bark before the pockets become large. A few deeper gum pockets of considerable size have also been found, tissue usually for a period of from 2 to 4 months. The removal of situated in the outer gummous zone beneath layers of wood % to i/4 of an inch in thickness, showing accumulations of gum under pressure. The gum, which is watery and clear when first formed, hardens as it comes to the surface, apparently through loss of water, and finally becomes brittle. On the surface the hardened gum is usually mahog- any to chestnut in color.^^ The gum accumulates on the surface in long narrow ridges (figs. 1 and 2a) or in oval masses, or runs down and collects in masses on the soil, according to the rapidity of its 10 Ridgway, Robert, Color standards and color nomenclature, 43 pp., Wash- ington, D. C, 1912. Bulletin 360] qUM DISEASES OF CITRUS TREES IN CALIFORNIA 375 Fig. 1. — Pythiacystis or brown-rot gummosis on lemon trunk. The tree is completely girdled the dead bark resulting from several infections starting near the soil surface. Eidges of exuded gum are characteristic. 376 UNIVERSITY OF CALIFORNIA — EXPERIMENT STATION formation and the dryness of the air. During periods of heavy dews and rains it gradually dissolves and disappears. The invading hyphae frequently die out rapidly behind the marginal fringe of advance, and quite often they die out completely over a part or all of this outer margin, so that the progress of the disease is checked or entirely arrested. Such cases are often found among trees having some power of resistance, especially among orange and pomelo trees; or where the weather conditions subsequent to infection become unfavorable to the parasite. In trees on which the disease has been present for a long time, the dead bark over the invaded portions dries, shrinks and cracks. The larger cracks are mostly vertical, with smaller horizontal cracks (fig. 2&). A thin layer of the wood immediately under the invaded bark will usually be found to be infiltrated with hardened reddish- brown gum which protects the under layers from rapid drying and to a considerable extent against the entrance of wood rotting fungi. On old sweet-orange trees, the invaded areas are usually less exten- sive and more restricted laterally than on the common lemon. There is usually less gum than on the lemon. In the orange there is a greater tendency for the invading fungus to die out and for the invaded area to become self -limited than in the lemon. Frequently the invaded areas on old sweet-orange trunks extend upward from the soil surface as narrow tongues of killed bark. On younger orange trees and frequently on older ones growing vigorously on heavy clay soils the disease may assume much the same characteristics as it does on the common lemon. INVESTIGATIONS INTO THE NATUEE AND CAUSE OF THE DISEASE Investigations begun in 1912 by the author^^ have led to the dis- covery that the disease is infectious and that the casual agent is a soil inhabiting 'Svater mold," Pythiacystis citrophthora, the same fungus which was previously described as causing brown rot of lemon fruits.^^ The relation of this fungus to the disease was discovered as a result of a series of experiments as follows: 1. Inoculation into sound trees with bits of diseased tissue trans- mitted the disease with all its characteristic symptoms (fig. 2). It was found, however, that only the diseased tissue from the marginal 17 Fuwcett, H. S., Two Fungi as Casual Agents in Gummosis of Lemon Trees in California. Month. Bull. Calif. State Comm. of Hort., vol. 2, pp. 601-617, 1913. 18 Smith, R. E. and others. The Brown Rot of the Lemon, Calif. Agr. Exp, Sta. Bull. 190, 1917. Bulletin 360] quM DISEASES OF CITRUS TREES IN CALIFORNIA 377 fringe of the killed bark of active lesions was capable of transmitting the disease. Tissue from places back of this margin toward the center of large lesions or from the outer gummous zone was incapable of inducing gummosis. Fig. 2. — Pylhiacystis or brown-rot gummosis on lemon tree. Produced by inoculation with diseased bark tissue. (a) Tree inoculated February 27, 1912 and photographed April 24, 1912. The large amount of exuded gum indicates the rapid development of a gummosis lesion. A majority of the trees in this same orchard had the same over growths at the union of stock and scion as observed in this illustration. (b) Same view as (a) on May 24, 1913, 15 months after inoculation. The gum first formed has been dissolved by winter rains, and the dead bark has dried and shrunken. Gum was exuding (farther around) at this time. 2. Culture tests made from pieces of bark from various places within and beyond the killed portion of the lesions revealed the presence of Pythiacystis citrophthora but usually only at the marginal fringe of what was subsequently called the invaded zone. This fungus usually could not be isolated from the central portion of the invaded zone and it was never found well out of the outer gummous zone. Isolations of this fungus were made at least 139 times from gummosis trees representing 30 different orchards in 10 different counties of California extending from San Diego on the south to Butte county on the north. It was isolated also from one locality in Arizona. 378 UNIVERSITY OF CALIFORNIA — EXPERIMENT STATION 3. Inoculations were made into bark of sound trees with pure cultures of this fungus and the disease was induced with all its characteristic symptoms (figs. 3 and 4a). Many repetitions gave the same results. Inoculations with large numbers of other fungi and bacteria found in the older portions of the invaded zone failed to cause the disease. The reason for the fact that only diseased tissue from the marginal fringe of the invaded zone was capable of trans- mitting the disease was now revealed. In this portion only, does the causal organism Pythiacystis citrophthora usually remain alive. 4. The same fungus was re-isolated 40 different times from 20 of the cases of gummosis produced by inoculation and again found to be alive only at the outer margin of the invaded zones, just as in the naturally occurring cases previously mentioned. The time elapsing between inoculation and re-isolation was from 1 to 12 months in different tests, and the fungus was recovered at distances of 20 inches or more from the original point of inoculation. One strain of this fungus isolated from a diseased tree at Whittier was inoculated into and re-isolated from three different trees in succession during a period of 3 years from 1912 to 1915. During this time the fungus lived in the bark of the three trees for periods of 5, 11, and 6 months respectively and between these periods in cultures for 2, 2, and 10 months respective^. Transfers from the original culture which was kept alive for more than 8 years on cornmeal agar medium were capa- ble of producing brown rot of lemon fruits when tested in 1921. 5. Inoculations were made also with bits of lemon fruits affected with brown rot and with the fungus Pythiacystis citrophthora isolated from diseased fruits, with the same results as those obtained by the use of bits of diseased bark or cultures isolated therefrom. This experiment served to show that the fungus previously known to cause brown rot of lemon fruits and the one capable of inducing this type of gummosis were identical. The detailed experiments on which these statements are based are being published in the Journal of Agricul- tural Research. RESISTANCE OF DIFFERENT SPECIES AND VARIETIES Among the citrus species and varieties that have been tested the common lemon has the lowest resistance to Pythiacystis gummosis, and the sour orange the highest. The sour orange usually is so resistant to Pythiacystis attack that even when the most favorable conditions are given by inoculation in wounds, there is only a slight gumming with rapid healing of the wounded tissue and with total failure to produce a diseased lesion. The sour orange is also highly resistant to all other infectious gum diseases of importance. Mere Bulletin 360] qx.tm DISE^VSES OF CITRUS TREES IN CALIFORNIA 379 CO •rt K tS <^ M T.) 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