Status of applied biological control of soil-borne plant pathogens

Soil Biol. Btochem.

Vol. 5, pp. 709-720.

Pergamon

Press 1973. Prmled m Great Britam

STATUS OF APPLIED BIOLOGICAL CONTROL OF SOIL-BORNE PLANT PATHOGENS GEORGEC. PAPAVIZAS Soilborne Diseases Laboratory, Plant Protection Institute, Agricultural Research Service, U.S. Department of Agriculture, Beltsville, Md. 20705. (Accepted 1 February 1973)

Summary-During the last 15 years a great amount of information has been accumulated on the ecology and physiology of soil-borne plant pathogens around the world. Despite this, very few cases of applied biological or cultural control have been reported. Although soil-borne plant pathogens are widely spread and economically important, only a small fraction of plant pathologists and soil microbiologists has devoted full time in the applied phases of biological control. The number of publications on applied control during the last 10 years in two journals surveyed is exceptionally small. The status of applied biological control of root diseases is considerably less favorable than the situation inentomology where much progress has been made during the last 10 years. The status of biological control (narrowly or broadly defined) of soil-borne pathogens is described here and several examples of applied control are cited. Future prospects for research on the ecology and biological control are also discussed.

INTRODUCTION

ago a paper by Sanford (1926) on potato scab (Streptomyces scabies) marked the beginning of a new era of soil-borne disease investigations, Sanford suggested that control of potato scab by green amendments was in fact a biological control, which he attributed to the action of antagonistic soil saprophytes on S. scabies. Sanford’s paper, as well as the work of other investigators of that era, exerted an extraordinary impact on the direction of research with soil-borne plant pathogens that was to follow for the next 50 years. Plant pathologists and soil microbiologists suddenly realized that it might be possible to suppress root diseases by manipulating the soil environment by appropriate crop rotations and soil management practices. Nothing has contributed more to summarize existing knowledge and to introduce new concepts than Garrett’s book on the ecology of root-infecting fungi (1956). Nothing has done more to stimulate research on the subject of biological control of soil-borne plant pathogens than the First International Symposium on the ecology of these pathogens at Berkeley in April 1963 (Baker and Snyder, 1965); and nothing has done more to popularize biological control than Rachel Carson’s Silent Spring (1962) which made certain segments of the population consider chemical control of pests as “the fatherless child of our technological age” (Compere, 1969). During the last 15 years a very considerable amount of information has been accumulated on the ecology of soil-borne pathogens: methods of isolation and enumeration; mechanisms of control and dynamics of inoculum in soil; definitions of the microhabitats; concepts of inoculum density, inoculum potential, and competitive saprophytic ability; enzymes and phytoalexins; and models of control and mathematical dynamics. The main aspects on principles and mechanisms have been admirably presented by others (Baker, 1968; Garrett, 1956, 1965; Mitchell, 1973; Wilhelm, 1973). It cannot be denied that all these studies have greatly increased our knowledge and our comprehension of several basic principles and ALMOSTHALF a century

709

7 I0

GEORGE

C. PAPAVIZAS

concepts. Equally, however, we have to admit that our hopes and expectations for biological control, that elusive gem of perfect control, have received various set-backs, disappointments and frustrations. No one has emphasized this more than Baker in his review of biological control mechanisms where he stated (1968): “During the last decade there has been great interest in and study of biological control of plant pathogens in soil. Among those who work in the area there is some doubt whether any considerable application or even modification of ancient established control measures has occurred.” Why have our numerous accomplishments in the field of applied biological control lagged behind our obvious needs and expectations? Why has all this high caliber research failed to lead us into formulating field procedures to alleviate or effectively control some of our soil-borne disease problems? Should we quit or reduce the emphasis of our efforts to control soil-borne diseases by cultural and biological means and focus our attention on genetic or chemical control? To raise these questions, however, for which I have no satisfactory answers, is not to declare that we have completely failed in our attempts to control soil-borne diseases by biological means. Should our research efforts be directed toward development of pesticides and resistant varieties only? Most plant pathologists that work with pesticides realize that most frequently it is difficult, nonprofitable, or inadvisable to use pesticides to control or reduce incidence of soil-borne diseases. Chemical control has had only limited success in controlling root pathogens in the past. Difficulties may arise from lack of suitable application methods or lack of effective chemicals; prohibitive cost of chemicals; and inactivation, decomposition or accumulation of undesirable chemicals in soils or in other habitats. Breeding for resistance to root diseases has not solved many problems possibly because most soil-borne pathogens are nonspecific and omnivorous and development of resistant varieties is a very difficult and long term project. What should, then, be our direction of research for the future? SURVEY

OF RESEARCH

ON APPLIED

BIOLOGICAL

CONTROL

Thus far we have no real census of root diseases. We do know, however, that none of the major economic crops escapes damage from soil-borne plant pathogens. Root rots, collar rots, wilts, seedling blights and damping-off take a heavy toll year after year. Economic losses from soil-borne plant diseases, caused by approximately 50 different genera of fungi and bacteria, may amount to more than one billion (109) dollars annually in the United States. Wilson (1968) in his recent book Roots: Miruclrs Below stated that “of the now duly recorded 2000 principal diseases of the 31 principal crops in the United States about 91 per cent are definable as diseases of roots or root spheres”. Although this figure may be exaggerated, there is no real doubt that a majority of the identified enemies of plants are associated with roots and the rhizosphere. Although soil-borne plant diseases appear to comprize an extremely important, widespread group of diseases of economic plants, only a small fraction of the American Phytopathological Society (APS) membership has identified itself with soil microbiology and root-infecting fungi during the 1963 and 1968 surveys of individual phytopathological interests (Fig. la). Less than 1 per cent in 1963 and less than 3 per cent in 1968 of the APS members identified themselves with biological control compared to 8 and 13 per cent with fungicides and nematicides, respectively. In another study of this type on the number of papers on soil-borne diseases published in Phytopatholoyy during the last 20 years only a small fraction had really anything to do with biological control per se (Fig. lb). With the exception of 1959, 1965 and 1968, less than 5 per cent of the papers were devoted to

BIOLOGICAL

CONTROL

OF

PATHOGENS

711

field research on soil-borne diseases. The majority of the papers were devoted to model systems and greenhouse or laboratory studies. Similar trends were observed when the papers on soil-borne diseases published in Plant L)isease ~~~o~~e~(PDR) during the last 10 years were examined (Fig. lc). A more detailed analysis of the papers on soil-borne pathogens in PDR showed that the smallest percentage of papers was devoted to biological or cultural control (Fig. 1d). E-Soil odcrobiol., sr&borne diseases, biol. control o- aihgical control

/ A- Total APS aembers~~ b Ne~~~~s

1

ial

“.“W

I 80

t

60 8

i 40 t

1.. I

A B

E

A

B

B

on soilborne diseases published

-Paw in RdNr

m

REPTRY.

of total.

C

0

6,’

(d)

-i

(c) i 46c

ae

+I11111 ,.I

20 -

0

SC I

e

.,.1

F

1961

9c I

ef

(964

IC I I f I996

BcR11FS

1910

FIG. I. (a) Some areas of expertise of the American Phytopathological Society membership expressed as per cent of total. (b) Number of papers on soil-borne diseases published in I’h~topathology from 1950 to 1970 (per cent of total) and number of papers on field research on soil-borne diseases (per cent of total on soil-borne diseases). (c) Number of papers on soil-borne diseases published in Plunf Disease Rvporrer from 1961 to 1970 (per cent of total) and number of papers on biological control of soil-borne diseases (per cent of total on soil-borne diseases). (d) Per cent distribution of papers on soil-borne diseases published in Piant Disease Reportrr in 1961, 1964, 1966 and 1970 in five categories. Letters under columns signify the following: BC, biological control; R, resistance; N, nematicides; F, fungicides; G, general papers.

A survey was also made of the projects coded under ~o~lbo~n~pfatzt ~~t~zog~ns, b~~l~gic~lthe Current Retrierial I?~~r#~ution System (CRIS) for 1969 and 1970. Only 30 per cent in 1969 and 13 per cent in 1970 of the prqjects in CRIS suggested the use of soil in “Approach” (Table 1). I do not desire to criticize the use of artificial media, synthetic solutions, or model systems of any kind, for they are useful and I have used them myself. It is, however, always to our advantage to avoid the use of soil? Admittedly,

cu~tz~ra~-c~nt~~l of

GEORGE

712

C. PAPAVIZAS

TABLE I. FREQUENCY OF ust OF SOIL SUGGESTED IN THE EXPERIMENTAL APPROACH OF PROJECTSIN THE UNITED STATES DEALING WITH SOIL-BORNE PLANT PATHOGENS, BIOLOGICALCULTURAL-CONTROL UNDER THE CURRENT RETRIEVAL INFORMATION SYSTEM(CRIS)

‘:0 of total

Year 1969

Projectssuggestinguse ofsoilin

1970

Projects Projects Projects

30 70 13 87

“Approach” not suggesting use of soil suggesting use of soil in “Approach” not suggesting use of soil

results will be more difficult to interpret if soil is used for experiments, but is it not where plants grow for our food supply? The status of biological control research in plant pathology contrasts sharply with the situation in entomology where in Canada alone about 25 per cent of their workers are specifically charged with the study of some aspect of biological control, either basic or applied. In entomology biological control is recognized as a discipline in its own right, with theresult that the entomologists have : (i) recognized specialists in the field; (ii) organized a number of administrative units in entomology in the world that specialize in biological control, among which are the Entomology Research Institute for Biological Control in Belleville, Canada, the Departments of Biological Control at Riverside and Berkeley, the Commonwealth Institute of Biological Control with laboratories or offices in Ottawa, Trinidad, Switzerland, California, India, Pakistan, and Japan, the Commission Internationale de Lutte Biologique in France, and, finally, the various units of biological control in the U.S. Department of Agriculture; and (iii) recently set in motion plans to organize the International Organization for Biological Control (IOBC) to promote biological control by itself or as a part of integrated control of pests. The first slate of candidates for the Executive Committee of the new Council of IOBC, proposed to be inaugurated in 1971, was comprised entirely of entomologists and zoologists (National Academy of Sciences, 1970). STATUS

OF

BIOLOGICAL

CONTROL

WHEN

NARROWLY

DEFINED

It would be a strenuous exercise in futility for me to review all successful cases of biological control of soil-borne plant pathogens and especially to enumerate the unsuccessful ones. In order for me at the outset to assess the potential for applied biological control in agriculture, I am confronted with the dilemma whether I should define biological control narrowly or broadly. Garrett (I 965) defined biological control “as any condition under which, or practice whereby, survival or activity of a pathogen is reduced through the agency of any other living organisms (except man himself), with the result that there is a reduction in incidence of the disease caused by the pathogen”. For my presentation, if I accept Garrett’s definition in a narrow sense, I will be able to cite only one successful case of biological control with field application. The only practical example that comes to mind is the inoculation of pine stumps with Peniophoru giguntru against infections of Forks unnosu.s. Spore infection of freshly exposed pine stump surfaces is not only confined to F. unnosus, but also to a few saprophytes or weak parasites like P. gigunteu. Rishbeth (1963) developed the first successful biological control through inoculation of stump surfaces with P. yiyanteu to have been adopted in practice. Large scale stump inoculations started in Britain in 1964. By 1970 the area of pine plantations in which P. giguntea is used reached about 40,000 ha. Inocula of the competitor may now be applied from a plastic container with perforations in the lid or the oidia of P. yigunteu may be

BIOLOGICAL

added to the oil inoculations are while F. annosus within the stump

CONTROL

713

OF PATHOGENS

used for lubricating the chain-saw blade, so that felling and stump achieved simultaneously (Artman and Stambauch, 1970). In this case, can be considered a soil-borne pathogen, the control operates entirely to forestall aerial inoculum of the pathogen.

STATUS

OF BIOLOGICAL

CONTROL

WHEN

BROADLY

DEFINED

I cannot give the deserved credit to biological control as an applied practice if I interpret Garrett’s definition in a strict sense. In a recent publication of the National Academy of Sciences (1968) entitled P/ant Disease Development und Control, coauthored by a number of specialists in the field, biological control has been considered as “an aspect of cultural control that involves primarily those practices that alter the biotic-abiotic condition from one that favors disease to one that discourages the accumulation of propagules and reduces the pathogenic activities of pathogens”. There is no better example of biological control in commerical practice today under the broad definition of the NAS book than the so-called “non-dirting” control of peanut (Arachis hypogaea) stem rot caused by Sclerotiurn rolfsii. The basic knowledge accumulated through many years of painstaking studies that S. rolfsii, a vigorous saprophyte, grows profusely on most fresh crop residue and that stem rot will result when colonized crop residue is close to a peanut plant has paid off, thanks to an ingenious way to avoid the disease, proposed and implemented by Garren and Duke of the U.S. Department of Agriculture Tidewater Research Station in Holland, Virginia (Garren, 1959; Garren and Duke, 1957). The “non-dirting” cultural control involves: (i) deep covering of all organic matter (potential food bases for the pathogen) present on the soil surface or in the upper 5-1Ocm of soil at the time of seed bed preparation; and (ii) non-dirting cultivation to control weeds in the row by means other than throwing soil around the base of plants during cultivation. The non-dirting weed control can be achieved by planting peanuts on a slightly raised bed and by using preemergence herbicides in band treatments. This type of cultural control is based on: (i) The observations by Taubenhaus (1919) leading to the recommendation of deep plowing; (ii) Tisdale’s (1921) discussion of the role of organic matter in the development of infection by S. rolfiii; (iii) the observations of Ciccarone and Platone (1949) in South America that throwing soil into the peanut row results in a marked increase in stem rot; and (iv) the theory of Boyle (1952, 1956) that stem rot may be effectively controlled by deep plowing to provide deep burial of organic matter and to control weeds without throwing soil on the peanut plant. Garren (1964) subsequently showed that infection of-peanut plants by S. ro@ii was less and yields greater with deep covering and non-dirting weed control than with surface mulching and dirting weed control (Fig. 2). Dr. Garren wrote to me recently that “Southern stem rot is being so effectively controlled by cultural practices which bury the organic matter well below the surface and which prevent the formation of new food bases in the peanut crown that it is useless to advertise soil fungicides for control of peanut stem rot”. Although we do not have a practical control of root rot and damping-off of many economic crops caused by Rhizoctoniu solani as yet, we do have considerable knowledge to devise one. The first spin-off of our studies at Beltsville on the competitive saprophytic colonization of R. solani (Papavizas and Davey, 1965) has occurred in The Netherlands. Our colonization method for detecting and estimating R. soluni is used in The Netherlands to estimate the inoculum density of the pathogen before planting potatoes that are to be sold later for “seed”. When the inoculum density is high, another field is used for potatoes. I should now like briefly to recall the following research accomplishments on R. solani:

GEORGE

714

C. PAPAVIZAS 3960

3550 ” ;

3170 = z

Ill -z E

1790

1 D

SOIL lnt67rtll7

FIG. 2. Per cent infected stand peanuts for the same 4-yr period following: DC-N = deep covering, deep covering, dirting; and SM-D 279-281.

by Sckr.~liurn ro//:sii at Holland, Virginia, non-dirting; SM.N = surface mulching. 1964. with permission

2410

M-0

and yield of Va. Bunch 46-2 and NC-2 The letters under the columns signify the = surface mulching, non-dirting; DC-D = dirting. (Adapted from Ph~ropurholog~~ 54, of K. H. GARRIY).

(i) A few years ago the State Extension Personnel of the San Joaquin Valley of California developed a cultural control of Rhizoctovlia root rot of beans by shallow planting (Leach and Garber, 1970). The soil is formed into beds on 106-cm centers; the seed is planted l-2.5 cm deep in two rows 30cm apart on each bed; and germination is promoted by subirrigation of the beds from irrigation water in the furrows. As a result, less than 2.5 cm of hypocotyl tissue is exposed to infection, and this only for short periods. (ii) Snyder et ul. (1959) showed that bean root rot caused by Fusariunn, Rhizoctonia, and Thie1aGopsi.s was reduced by adding to soil amendments of high C:N ratios such as mature barley, wheat straw, corn stover or pine shavings. (iii) In 1960 (Davey and Papavizas, 1960; Papavizas and Davey, 1960) we showed that green or dry corn and oats were the best amendments for control of Rhizoctonia root rot of bean. Corn and oats stimulated the highest number of streptomycetes antagonistic to the pathogen and suppressed its saprophytic activity in soil (Fig. 3). In 1969 Manning and Crossan (1969) assessed the effects of green and mature plant amendments on hypocotyl rot of snapbeans (Phaseolus uulyuris L.) in the field. Green and dry corn amendment significantly decreased the disease. The corn effect persisted for almost a year in the field. What we need now is not only further basic work on R. soluni, but an ingenious but practical exploitation of the already known facts in the field concerning this pathogen, similar to that reported for S. rolfsii (Garren, 1959, 1964; Garren and Duke, 1957). It may be possible to utilize the information obtained through basic and applied research (Davey and Papavizas, 1960; Leach and Garber, 1970; Manning and Crossan, 1969; Papavizas and Davey, 1960; Snyder et ul., 1959) to set up a workable scheme of control by combining methods of control such as those already discussed. This kind of research to integrate various methods of control of R. solani is now being performed in the Soilborne Diseases Laboratory of the Plant Protection Institute at Beltsville. It would be another exercise in redundancy for me to attempt a complete review of the status of diseases controlled or alleviated by crop rotation, cultural practices or crop management. In practice today highly specialized pathogens are kept under a fair degree of control by use of crop rotation and soil management practices that retard the build-up of the pathogen. Several review articles (Curl, 1963 ; Glynne. 1965 ; Stevens, 1960) have

BIOLOGICAL

CONTROL

OF

715

PATHOGENS

(a)

1

3

5

7 WEEKS

10

100

0

.

Percent colonization

(b) 5

p z 40 J z x 20

2; II 15

0

Z z

0 CORN

OATS

BEANS AMENDMENT

SUO.CR.

NONE

FIG. 3. (a) Effect of green amendments and time of incubation before planting in sandy soil naturally infested with Rhizoctonia solani on infection indices of 3-week-old bean seedlings [Mean severity rating on surviving individual plants on a scale of 0 (no disease) to 5 (hypocotyls completely girdled)]. (b) Competitive saprophytic colonization by R. solani of buckwheat (Fagopyrum esculentum Moench) stem segments buried in amended and nonamended soil, and rhizosphere antagonistic streptomycetes enumerated 8 weeks after addition of amendment to soil naturally infested with the pathogen (Adapted from Phytopathology 50,516-522, 1960).

listed many diseases caused by soil-borne pathogens in which crop rotation provides the basic means of control or of reducing the severity of root rots and other soil-borne diseases. Crop and soil management practices have on occasion been dramatically effective, but they are often very erratic and reveal great voids in our knowledge of scientific principles and in the advancement of the arts of crop management. To illustrate the present status of biological control further, I will mention briefly a few more cases of successful control that have resulted from an extraordinary amount of basic work: (i) The successful alleviation of the take-all disease of wheat caused by Ophioholus yrurninis by manipulating the time of fertilization and the kind of fertilizer (D. M. Huber, personal communication). Application of N in the fall and planting of wheat in the spring resulted in increased disease and decreased yields. Application of the same kind of N just before seeding in the spring greatly reduced take-all and increased yields. In Huber’s experiments addition of (NH&SO, at 130 kg of N/ha decreased the incidence of take-all whereas NH,NO, added at the same amount increased it. (ii) The effectiveness of a 2-yr rotation in reducing the incidence of Verticillium wilt of cotton in the Mississippi Delta area (Hinkle and Fulton, 1963). Three years of alfalfa sod or 3 yr of fescue-white clover sod produced some of the highest cotton yields. (iii) The alleviation of the Phymatotrichum root

716

GEORGE

C. PAPAVIZAS

rot of cotton in Arizona by a I-yr rotation using Papago peas as a winter green-manure crop advocated by Streets (1969). As this permits continuous cotton cropping with high yields, it has met with growers’ approval. Limited space does not permit me to discuss the now classical work performed by many investigators on P. ~~~~i~~r~~?l that preceded Street’s recommendations and the recommendations by others for controlling this pathogen by deep plowing, green manuring and crop management. (iv) The encouraging results obtained by Green (1967) on the control of Verticillium wilt of peppermint (Mentha pipe&a L.) in Indiana muck soils following 5 years of continuous cropping with corn or after reed canary grass (P~~ulffrjsarl~~td~~~ce~L.). Little reduction in wilt incidence occurred following potato or soybean. The control was attributed by Green to the germination of microsclerotia of I/. albo-atrum in the rhizosphere of corn and to its apparent inability to colonize the corn root system. (v) Burke’s observations (1968) that the yield-depressing effects of Fusariurn root rot of bean were practically eliminated in infested soil by subsoiling to about 50 cm immediately before planting. Subsoiling did not control the pathogen, but permitted extension and regeneration of bean roots through the plowed soil layer into the subsoil. Bean roots infected by F. solani f. sp. phase& generally are damaged more by the pathogen in compact soils, which impede root growth, than in soils more easily penetrated by roots. Burke observed that plants in the subsoiled rows had deep-penetrating and larger root systems than those in rows not subsoiled. The more voluminous and vigorous root system promoted by subsoiling permitted more efficient use of soil moisture and nutrients than those in non-subsoiled plots and eliminated or reduced the yieId-depressing effects of the disease. (vi) The work of Weinhold et al. (1964) who found that potato scab incited by S. scabies is effectively prevented in the field in California by growing soybeans as a greenmanure crop in the fall after potato harvest and turning the green crop under before planting potatoes in the spring. A barley cover crop used as a green manure increased the disease to a level twice that of the unamended control. Weinhold and Bowman (1968) found that ~ac~~~~~subt~l~.~,a bacterium producing an antibiotic sjmilar to bacitracin, was abundant in plots amended with soybeans or barley. Soybean tissue extract, however, provided a more suitable substrate for antibiotic production by B. subtilis than barley tissue extracts. The potato scab organism was more sensitive to the antibiotic produced by this bacterium than most nonpathogenic Streptomyces spp. From the evidence discussed on the status of control by crop rotations and greenmanuring I might add that while the outlook for successful exploitation of control by crop management is excellent and highly intriguing, the studies required to implement it are complex and require new techniques, imagination and ingenuity. Behind cultural or biological control there is an endless series of problems to be solved in applied microbial ecology. Such control requires complex knowledge and comprehension of each ecological sit~lation-and there are no shortcuts. FUTURE

PROSPECTS

My brief coverage of the present status of biological control, no matter how narrowly or broadly one defines it, will have little heuristic value unless it is followed by at least a brief attempt to discuss some new areas for future research or potential control. Recently we have obtained evidence (Lewis and Papavizas, 1970,1971; Papavizas, 1966) that cruciferous plants may be subjected to microbial decomposition in soil with the formation of volatile S-containing compounds such as methanethiol, sulfides and isothiocyanates. Sulfides and isothiocyanates were extremely toxic to Aphanomyces euteiches and A. cochlioides. Although almost all crucifers may grow profusely and liberate toxic volatiles upon decomposition,

BIOLOGICAL

CONTROL

OF PATHOGENS

717

they have not as yet been utilized as cover crops or in rotation systems. Special categories of plants such as crucifers, as well as other higher plants known to contain antimicrobial substances, will undoubtedly become interesting targets for future research. Infesting seeds or other special surfaces with antagonists to reduce disease will come again into prominence. Several advances in this respect have been reported recently. Chang and Kommedahl(l968) reported success in biological control of corn seedling blight caused by Fusarium roseum f. sp. cerealis “Graminearum” by coating kernels with Bacillus subtilis or Chaetomium globosum. Coating kernels with antagonists improved stands in the field and greenhouse and yield of corn was increased from 7 to 20 per cent in the field, in comparison with nontreated seed. Aldrich and Baker (1970) presented evidence that B. subtilis, isolated from the rhizosphere of carnation and used in suspension to coat cuttings, reduced stem rot of pink carnation (Dianthus caryophyllus L.) caused by Fusarium roseum f. sp. dianthi. Appreciable biological control was obtained whether the antagonist was applied in a dip or incorporated in the rooting medium. This method of biological control may become very practical and useful for the control of Fusarium stem rot of carnation. The role of ectomycorrhizae as biological deterrents to pathogens of feeder roots will be increasingly studied in the future. Great impetus to this kind of research has been recently given by the elegant studies of Marx (1969) and Marx and Davey (1969) who found that ectomycorrhizae of shortleaf (Pinus echinata Mill.) and loblolly (Pinus taeda L.) pine seedlings may serve as deterrents to attack by Phytophthora cinnamomi by virtue of antibiotics produced by the ectomycorrhizal fungi. INTEGRATED

CONTROL

It is possible that plant pathologists and soil microbiologists, in immersing themselves in the exciting, challenging and intriguing prospects of biological and cultural control of soil-borne plant pathogens during the last 15 years, have neglected the possibilities of an integrated or multipurpose approach to root disease control. Irving (1970) recently defined integrated control as a “compatible system of control in which various methods are used in proper sequence and timing so as to create the least hazard to man and the environment and to permit maximum assistance for natural control”. Integrated control, a relatively new catch phrase for a down-to-earth approach derived from the modern-day environmentalists’ thesaurus designates the approach where all- methods of biological control (tolerant varieties, green-manuring, deep plowing, sanitation, amendments and residues, seedbed preparation, plant-spacing, nutrition, and other cultural practices) may be brought into operation to reduce pathogenic activities to a tolerable or permissible level, with chemicals applied only when absolutely necessary. It is obvious that integrated control is no more than a blending of chemical and biological control (including resistance to disease) with a continuous struggle to shift emphasis from the former to the latter. From the standpoint of practical, economic control, it is immaterial whether reduction of pathogenic activities is the result of reduction of inoculum density by the integrated components of control or whether it is merely some kind of host escape without a reduction in inoculum levels of the pathogen. One of the relatively early examples of simple integrated control of a soil-borne pathogen is the suppression of Armillaria mellea mediated indirectly by fumigating the soil with nontoxic concentrations of CS, (Bliss, 1951). The fumigant stimulated the multiplication in soil of the antagonistic fungus Trichoderma. A. mellea was destroyed in soil by the antibiotic action of Trichoderma by the end of the 7-day-fumigation period, but was not complete until about 24 days later.

718

GEORGE

C. PAPAVIZAS

Exciting data are now accumulating that by altering the microbial flora of the soil with very small dosages of certain selective chemicals we may be able to stimulate another type of microbial flora of substantial antagonism to troublesome root pathogens. Recently, Pinckard and associatesin Louisiana (1970) found that field applications of the monosodium salt of hexachlorophene at 280 g/ha to cotton plants and soil resulted in significant increases in disease control. The evidence suggested that the observed field control of several cotton diseases with amounts of the chemical nontoxic to the pathogens (Rhizoctoniu, Pythium, Phytophthora, and Fu.sariunz) is indirect, and related to the ability of the hexachlorophene to alter the ecological balance of the soil. A parallel phenomenon was reported recently by Stankova-Opocenska and Dekker (1970). Pq’thium debaryanunz, which causes damping-off in many plants, is insensitive in vitro to the systemic fungicide 6-azauracil (Azu) even at 1000 parts/lOh. Dekker and StankovaOpocenska obtained protection of cucumber (Cucu~is satiuus L.) seedlings against this pathogen by soaking the seed in a solution of 1 part/lo6 Azu, but not when the seed was soaked in an aqueous solution of 10 or 100 parts/lo’. Azu at 1 part/lo’ changed the microflora in the rhizosphere of developing seedlings; bacteria increased and fungi decreased. The authors suggested that the control was obtained via the increased microflora at 1 part/lo’ but not at 10 or 100. A final point that needs to be stressed about integrated control is that this approach may be directed against more than one pest. According to Todd (1971), “a multi-purpose treatment might be simply defined as one that provides control for two or more diseases”. Cultural practices and use of tolerant varieties can be effectively used with chemical practices such as seed treatment or in-furrow applications of minimal amounts of pesticides to supress more than one pathogen. Factorial experiments by Nusbaum and Todd (1970) and Todd and Nusbaum (1969) involving various combinations of control practices have shown the relative roles of host resistance or tolerance, cultural practices and soil chemical treatment in complex disease situations such as those of tobacco caused by root knot nematodes, black root rot (Thieluaiopsis busicola), black shank (Phytophthoru purasiticu var. nicociunur) or southern bacterial wilt (Pseudomonus solunuceururn). For varieties susceptible to black shank or bacterial wilt, either chemical soil treatment, crop rotation or a combination of these practices was inadequate for appreciable control. Performance of tolerant or resistant varieties, even those with high levels of resistance, was greatly improved either by rotation or soil treatment and especially by a combination of the two methods. From the definition of integrated control and the limited number of examples pertaining to soil-borne diseases that can be found in the literature, it is evident that this kind of control may become prominent in the future. Before a successful start can be made with this program, however, an extraordinary amount of work has to be done in the field to untangle some of the immensely intricate associations pertaining to the ecology of the host and the pathogen, and the relation of the two to the total environment. The preceding examples of integrated control of soil-borne diseases show that plant pathologists are just beginning to utilize integrated control as a field practice to control soil-borne plant pathogens. In sharp contrast, the entomologist have already advanced this concept, and applied it to control insects in the field, in a considerably larger scale than plant pathologists. According to Compere (1969) the integration of chemical and biological controls of insects has started in entomology “before the present generation of entomologists was born”.

BIOLOGICAL

CONTROL

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PATHOGENS

719

CONCLUSIONS

Even the integrated or multipractice disease control approach, however, will not be farsighted and wise unless we continue, or even increase, our cogent efforts to obtain complete knowledge of the biology and epidemiology of soil-borne diseases and of the ecology of the crop plants and the parasites involved. No other dictum can conclude this review more appropriately than Christie’s conclusion on nematode research (1959): “It would be a mistake to infer from these rather unimpressive observations and experiments that contrived biological control of plant nematodes is either impossible or impractical. This approach to the nematode problem offers a fascinating field for research that might yield important practical results but probably not until after the patient acquisition of considerable basic information about soil biology. Even if it failed in its main purpose, the acquisition of such information could scarcely fail to be of enough practical value to justify the effort”. REFERENCES

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