VOL. 44, No. 8, AUGUST 1963 499

Biometeorology and Plant Disease

RICHARD D. SCHEIN

Pennsylvania State University

In mid-1962, publications of portions of Rachel in what intensity that threat is going to present Carson's Silent Spring in the New Yorker focused itself, and to know these things demands a more attention on the widespread usage of chemicals in accurate knowledge of complex interactions of modern agricultural practice. The insecticides re- parasite, host, and environment. ceived the largest portion of the indictment, but Thus, I would like to discuss that part which fungicides and other materials used in the control biometeorological investigations play in laying the of infectious plant diseases were not ignored. foundations for proper forecasting of plant disease Plant pathologists concerned with plant disease development. To avoid error in interpretation, I control have, for years, realized that they operate will work within the definition that biometeorol- in a twilight area between applied chemical con- ogy is a branch of ecology which studies the inter- centrations so high they damage plants, as well as relations between the chemical and physical fac- humans and animals, and so low they do not con- tors of the environment and living organisms. trol parasites. The federal and some state gov- Its bailiwick ranges from the bottom of the rhizo- ernments have regulations to guarantee residue sphere to the highest levels of the atmosphere levels probably not injurious to humans and ani- where pollens and spores may be found. Biome- mals at ingestion. These matters, and commen- teorology is further concerned with manmade en- tary on faults of Miss Carson's position and con- vironments. It is an interdisciplinary field involv- clusion, have been the subjects of book reviews, ing a wide range of atmospheric and biologic articles, and somewhat official rebuttals from the sciences. To me, it is autecology, redefined. agricultural chemical industry in its trade journals. This definition acknowledges that biometeorol- But no matter how the use of chemicals is ration- ogy is a branch of biology, that some important alized, there is considerable truth in the opinion biological responses are a function of the environ- that, in any given season on any given crop, more ment, and that ecological characterization of these chemicals are used than might actually be neces- responses constitutes biometeorology. We should sary. note, however, that those situations in which the Plant pathologists submit that without the living organism has effects on environment chemicals they could not maintain the quantity (which might be called 'feedback'), including its and quality of agricultural production required, own, are also of concern to the biometeorologist. any more than a physician could curb human disease without prescription formulae. But ex- 1. Some general comments on plant disease cessive use of chemicals is a fault in the art of plant disease therapy, for its practice is still largely Plant disease originates from many causes— empirical. Plant diseases are remarkably, inextri- weather, soil and nutrition factors, bacteria, fungi, cably, weather dependent. In the absence of quite viruses, animals, and genetics—but, regardless of precise knowledge—disease by disease—of this incitation, weather and the host's environment dependence, forecasting of occurrence is far from play large roles. My remarks will be mostly perfect. Today's regimens for the control of plant about fungous diseases, not only because great at- disease make certain the chemicals are present tention has been and will continue to be paid to when the disease threat presents itself. What we them, but because they make good subjects to il- want to know—need to know—is when, how, and lustrate various points. 1 Contribution No. 305 from the Department of Botany Plant disease development has a sequence, and and Plant Pathology, The Pennsylvania State University. that sequence is greatly conditionable. We first Presented at Symposium on Biometeorology, American recognize that host and parasite each has a genetic Association for the Advancement of Science, Phila- delphia, Dec. 27, 1962. system which determines the range, rapidity, and

Unauthenticated | Downloaded 09/27/21 11:13 PM UTC 500 BULLETIN AMERICAN METEOROLOGICAL SOCIETY quality of its actions. Each of these systems is riod. Several biometeorological processes are subject to change through normal genetic mech- operative. A plant's predisposition to be dis- anisms. Within these genetic bounds, the game is eased after inoculation depends, in part, on inter- played, the organisms responding variously to the actions during Period I with nutrients; soil tem- physical environment, and, in the pathological perature, moisture, and reaction; atmospheric process, they respond to each other. The number temperature, moisture, and constituents; and light and degree of these interactions among host, para- quality, intensity, and perhaps photoperiod. site, and environment determine when disease oc- At point II the first inoculum arrives, for our curs, its quantity, its severity, and its epidemic fungus, as spores. The numbers (density of in- potential (or how fast it will advance). oculation), viability, genetics, and potential infec- Thus, Large's [1] equation for the progress of tivity of this inoculum is important. How some potato blight of these become part of biometeorological study will be partially covered under Period V. % = Ca(A-a) The arrival and deposition of inoculum at II is meaningless unless those spores have found sus- in which C is a constant, a is the proportion ceptible hosts and can germinate and their tubes of susceptible tissue that is infected, A is total penetrate the hosts and establish infections. susceptible tissue, and t is time, and which says Luckily (from man's point of view), this is one that the rate of disease development is propor- of the weakest links in the disease production tional to the product of the proportions of dis- chain; here is a place where environmental de- eased and healthy tissues, can be rewritten by pendencies are quite strong. Most fungous spores Van der Plank [2] as have an obligate free moisture requirement for rJr germination, germ tube growth, and penetration ^ = kx(l-x)f(T,H,S...) (Period III). These processes are also tempera- ture dependent and so the interaction of time span in which x — a above; A becomes unity and and temperature of moisture on leaf surfaces be- f(T,H,S,...) is a function of temperature, humid- comes important. ity, host susceptibility, etc. The Period III situation may be further com- The environmental dependence of a generic fun- plicated by light effects, by the chance that a gous disease can be illustrated as in Fig. 1, the germ tube can 'find' an infection court, by the sequence of development in time. availability of such infection courts, and by the The line starts with seeding, or the beginning age and physiology of hosts. of host growth, and proceeds for a time during It is to protect against these events of Period which the seed germinates and/or growth occurs III that most fungicides are applied before the and susceptible tissue is produced. Sometime moisture period occurs, since the chemicals are during its life, pathogens, capable of inciting dis- prophylactic, acting as a barrier between the host ease, reach the plant's leaves (inoculation). This and parasite. Plant disease-protection regimens segment (I) we can call the pre-inoculation pe- and forecasting techniques are largely designed

FIG. 1. The sequence of development of fungal plant disease.

Unauthenticated | Downloaded 09/27/21 11:13 PM UTC VOL. 44, No. 8, AUGUST 1963 501 to make certain the plant is protected when the [6], and many others. The second reference con- disease threat presents itself. tains a bibliography of over 400 citations to work Period III is usually short, perhaps 2-48 hours on these matters. in length (depending on organisms and weather) The outlined process is obviously sequential; but it can reoccur as frequently as favorable one process is dependent on the success of previ- weather, once inoculum is available or begins to ous ones. Meteorological variables affecting the arrive. Successful penetrations and infections processes vary in their primacy; free moisture now enter an intimate relationship with the host may be most important at one stage, temperature (Period IV), and, logically, all of those factors at another, and wind at a third. But the con- playing roles in host development in Period I may clusion I want to draw seems obvious. The com- be operative. plexity of disease development derives from the We must add here the interactions of the ge- complexity of the interactions involved. Fore- netic-physiologic systems of host and parasite. casting, to be really accurate, must be based on These interactions determine the rate of coloniza- precise knowledge of a fantastically complicated tion of the host and the character of the interac- ecology. tion and thus, the time of appearance, character, and, perhaps, number, of symptoms. Here is 2. A word about epidemics where the disease is felt by the plant and by its producer. The word "epidemics" means in or on people, These same interactions and factors affect the so we are not quite correct when we talk of epi- time of occurrence and character of fungus fructi- demics of plant diseases, or of epidemiology—the fications : in our example, the production of spores. science comprising the study of epidemics. We And, the numbers of spores produced—per lesion, have a word in botany for this unarrested spread per field, per farm or larger area—have a marked of disease in plants—epiphytotic. Unfortunately, effect on subsequent cycles and the rate of devel- 'epiphytology' which should logically mean the opment of the epidemic. Epidemics do not occur study of establishment and spread of disease in unless there are several repetitions of the cycle. plants—was given a restricted meaning some 50 During the time consumed, plants may also be years ago. Students of plant pathology were then producing more susceptible tissue as a function of taught, as they are often taught today, about the the environment. The roles played by physical etiology and the epiphytology of diseases. In in- environment, time, the 'incubation' period, and the fectious diseases, etiology dealt with the infectious rates of disease development are acknowledged agent—the fungus, bacterium, or virus—and with by Van der Plank in his current work on the its responses to environment. The effect of other analysis of epidemics [2]. Waggoner has added factors on disease development was covered under statements concerning the 'danger' to which a sus- epiphytology. Obviously, if one is interested in ceptible field is exposed and considers the relative the interactions of all factors, including the pri- effects of local spores and foreign spores in mary agent, in the establishment and spread of abetting the epidemic [3]. plant disease, this definition of epiphytology is For repetitions of the cycle to occur, the formed too restricting. For years, and even today, plant spores must escape the fructification, be trans- pathologists have referred to the "etiology and ported, and be deposited on other susceptible epiphytology" of a disease. For simplicity, many leaves (Period V). Here we enter the field of of us have taken the expedient way and adopted aerobiology (or aeromycology) and must consider the medical term epidemiology.2 a) the character of fructifications and of spores as The kind of epidemic I am using for illustration they affect active and passive spore release, b) is one that occurs in a single season (although it boundary layer factors as they affect escape and need not) and which has a shape similar to that deposition of spores, c) matters of turbulent shown in Fig. 2. Beginning with the first infec- transport and dispersion, d) the probability of tion in a population of plants, there is a long 'finding' a new host, and e) environmental effects period (the lag phase) during which the infection on spore viability during these events. This is 2 I am indebted to Dr. D. N. Welch of the Plant Pa- obviously a fertile area of biometeorological in- thology Department of Cornell University and to Dr. vestigation because of interactions with wind, Clifford Wernham of the Pennsylvania State University moisture, temperature, solar radiations, etc. Read- for some correspondence in 1956 which clarified the posi- tion of Dr. H. H. Whetzel of Cornell, who evidently ers are referred to the recent publications of placed the restricted meanings on etiology and epiphytol- Waggoner [3], Gregory [4], Pady [5], Schrodter ogy.

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(asexual, usually) capable of having increased the available inoculum, as well as disease extensity and intensity, to the point that the epidemic is at the threshold of its exponential phase. Through the great amount of research conducted since 1925 in many countries in Europe and the Americas [8, 9], forecasting of the late blight disease of potato has been established on the basis of actual (not probable) occurrence of temperature and moisture conditions (including atmospheric hu- midity) conducive to sporulation of the parasite (Period V), germination of zoospores and spo- rangia, and the establishment of infection loci (both in Period III). These are forecasts of the first, really visible disease occurrence, about 0.1 per cent of foliage affected, and thus involve the assumption FIG. 2. The development of a plant disease epidemic. that the lag phase has reached an end. Obvi- ously, such forecasts are not made early in the becomes more general (on individuals and in the season while the lag phase is in progress. These population). During this previsible period, the forecasts call for fungicidal applications to pre- inoculum level and potential increase. (This is vent further repetitions of the cycle and to not the inoculum potential as defined by Garrett thereby interrupt the exponential phase. [7].) By the time the infection is general enough Lima bean downy mildew, incited by a related to be noticeable, the inflection of the curve is near, parasite, is forecast on the same basis, but the called variously the threshold or outbreak, or on- forecasts are modified when air temperatures of set of the epidemic. Development thereafter is 85F or higher occur on the day following a exponential. This is the true epidemic phase. critical moisture period. The significant point We have almost no data on the lag phase of epi- here is that this technique acknowledges that demics for at least two reasons: 1) Since epi- events in Period IV can strongly affect the course demiology is a population study, disease extensity of disease by modifying what happened in Period must be assayed over a large area or at least a III. large population, and, in these early stages, the Other techniques also acknowledge that the ex- concentration of disease, whether assayed as le- ponential phase cannot be reached without the lag sions, or leaf surface involvement, or other index, phase—that is, unless several parasite generations is so dilute as to be practically unassayable. 2) did occur to provide further inoculum. They also The spores produced by the pathogen and re- acknowledge that this build-up, usually not noticed leased into the air are so diluted in the tremendous or even noticeable, demanded repeated favorable air spora as to be unidentifiable and/or uncount- environment. An excellent example is a tech- able. nique developed in Oklahoma for forecasting wheat leaf rust. The disease is forecastable when 3. A resume of some forecasting techniques amounts of overwintered inoculum can be esti- mated, and this can only be done when early Plant disease forecasts, as predictions of danger spring weather has favored early buildup of in- or probability of ensuing development, must ac- oculum so that, by April 1, sufficient amounts of knowledge the sequential processes of disease de- inoculum are available to start the exponential velopment and the contributions of the various phase and enough time remains for development interactions to the final product. But currently, of that phase. Significantly, another element con- to be practicable at all, forecasting techniques do sidered in this scheme is environment favorable not take into account all interactions; rather, they for prolonged growth of susceptible plant tissue, are based on as few as possible critical processes. Period I. Forecasting techniques already developed are Apple scab disease forecasts are of another of several types and include some basic assump- genre in that they acknowledge that, in this case, tions about the lag phase. Most commonly, they there is no appreciable lag phase. This is so be- assume the presence of initial inoculum and cause the potential inoculum sources—fungus the occurrence of several parasite generations fructifications on last year's leaves on the orchard

Unauthenticated | Downloaded 09/27/21 11:13 PM UTC VOL. 44, No. 8, AUGUST 1963 503 floor—are apt to be so large as to be sufficient to We have never really studied the lag phase, cause very high amounts of bud disease in the mostly because we cannot really see and measure first cycle. Two factors are assayed—usually either the disease or the inoculum status during temperature and moisture. These are relevant this period. Yet, we certainly recognize that the to ascospore liberation and germination and bud exponential phase cannot occur without its prede- development to a susceptible stage. The effects, cessor. How to study it is a problem, but the then, are in Periods V, III, and I, respectively. recent development of the concept of r by Van der The French technique actually relies on records Plank allows some exciting possibilities. of spore trapping. We know too little about effects of crop age, Interestingly, one disease, bacterial wilt of sweet phenology, energy budget, and infrared heating corn, can be forecast on the basis of winter tem- of plants as modifiers of the disease and inoculum perature high enough to allow high survival rates development rates. of the pathogen's insect vector. We know far too little about matters of aero- biology—that is, about spore release, transport, 4. How can the art be improved? dispersion, and deposition—and about what hap- pens to propagules biologically during these This brief resume of a few forecasting tech- events and processes. To quote a statement by niques (about a dozen others exist) is meant to P. H. Gregory, "Our knowledge of the terrestrial illustrate the point that most rely on information air spora is fragmentary in the extreme. . . . relevant to only small segments of the disease de- There is a heap of accumulated data. . . . Here velopment schematic. Some techniques in certain and there are intriguing suggestions of phe- places are much more developed and much more nomena ; but many of the data are uninterpretable. accurate than others, but, at present, none are . . ." We will need wind tunnel work, inter- really perfectly developed. national progams, new techniques, and the coop- Forecasters currently take the conservative eration of experts in fluid dynamics. The sta- position; they are, for the most part, predicting tistics of such studies will be staggering. How- the probable beginning of the exponential phase ever, epidemic theory will lag until such work is and have little information about the lag phase. accomplished on a rather large scale. Assuming that inoculum levels, host phenology, As advanced information begins to accumulate, and other items are 'ready/ occurrence of disease- we will be able to construct epidemic models inte- conducive weather means a positive forecast and grating all of those complicated, interdependent the sprays go on. Thus, is it assured that crops processes. Besides the obvious scientific value of are protected during all possible danger periods such biometeorological endeavor, several other after a certain starting point. products are promised. But I must not leave the impression that ad- The plant pathologist will be in a better posi- vancements are not occurring. The current re- tion to protect the world's food and fiber supply, liance on actual observance of conducive weather making his contribution to the better feeding and is not satisfactory, and efforts are being made clothing of a growing world population. to tie disease forecasting into synoptic weather The forecaster will be able to make negative forecasts. As meteorological forecasting im- forecasts which say, "Don't Spray." But con- proves, aided by such techniques as radar, satel- sider the responsibility! He must be sure before lites, and complete and rapid communications he can make a negative forecast. If he is wrong, networks, the disease forecaster can improve his the epidemic will soar away on its exponential efforts by using the information. Then, rather flight. Growers and public alike will profit from than making a forecast after the first dangerous negative forecasts by saving large sums of money weather, he will make it before. and because the amounts of chemicals used for But I think the greatest efforts will be made in any particular crop may be reduced. the biology and theory of epidemics. Since the If Miss Carson indicts us for irresponsibility, war, there is a renewed interest in these matters, and the food and agricultural chemical industries specifically about epidemic theory, about spore respond with statements that things are not as transport, dispersion, and deposition, and about bad as they seem, and we must do as we do to the probability of a crop being endangered by in- satisfy demands, I hope this presentation deline- oculum from outside sources. This interest must ates one other approach to disease control—the be increased, augmented, and developed with the complexity of the problems needing solution, and sophistication it deserves. what some plant pathologists propose to do about it.

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REFERENCES 5. Pady, S. M., and C. L. Kramer, 1960: Kansas aero- mycology. VIII. Smuts. Phytopathology, 50, 1. Large, E. C., 1945: Field trials of copper fungicides 332-334. for the control of potato blight. I. Foliage pro- 6. Schrodter, H., 1960: Dispersal by air and water-flight tection and yield. Ann. appl. Biol., 32, 319-329. and landing. Plant pathology, An advanced trea- 2. Van der Plank, J. E., 1960: Analysis of epidemics. tise Vol. III. (J. G. Horsfall and A. E. Dimond, Plant pathology, An advanced treatise Vol. Ill, eds.), New York and London, Academic Press, (J. G. Horsfall and A. E. Dimond, eds.), New Inc., pp. 169-227. York and London, Academic Press, Inc., p. 235. 7. Garrett, S. D., 1956: Biology of root-infecting fungi. London, Cambridge University Press, 196 pp. 3. Waggoner, Paul E., 1962: Symposium on weather and 8. Cox, A. E., and E. C. Large, 1960: Potato blight epi- plant disease. Weather, space, time, and chance demics throughout the world. Agric. Handbook of infection. Phytopathology, 52, 1100-1108. No. 174, Agric. Res. Serv., USDA, Washington, 4. Gregory, P. H., 1961: The microbiology of the atmos- D. C, 230 pp. phere. London, Leonard Hill [Books] Limited, 9. Miller, P. R, and Muriel O'Brien, 1952: Plant disease 251 pp. forecasting. Botan. Rev., 18, 547-601.

(Continued from ANNOUNCEMENTS, page 488) mospheric variables on short-term growth and develop- ment of plants; c) The influence on microclimate of vari- American Society of Agronomy to Meet ations in crop structure brought about by crop breeding in Denver or management; d) Agroclimatological studies: probabil- The American Society of Agronomy and affiliated soci- ity of occurrence of soil-moisture deficiencies, etc. Re- eties—the Crop Science Society of America and the search involving other areas of interest will be con- Soil Science Society of America—will meet in Denver sidered. Good research facilities are available and an on 18-22 November. The meetings will be held at the excellent opportunity to become competent in the use of Denver Hilton Hotel. the latest techniques of measurement and data processing The general theme of the meeting will be Pan-Ameri- is afforded to all students. can Agronomy. Some 500 research reports by sci- Those interested in the program may write for infor- entists from every State and several foreign countries mation on assistantships and other details to Dr. K. M. will deal with improvement of crop and soil conditions King, Chairman, Committee on Agrometeorolcgy, De- for better production. Conditions in Pan American partment of Soil Science, Ontario Agricultural College, countries will be discussed by leading Latin American Guelph, Ontario, Canada. agronomists and United States scientists with experience in these countries. Practical research, as in the past, NSF Senior Postdoctoral Fellowships will receive the emphasis in most of the discussions. in Science Further information about the meetings may be ob- tained from the American Society of Agronomy, 677 The National Science Foundation has announced its South Segoe Road, Madison 11, Wis. 1963 Senior Postdoctoral Fellowships. Approximately 100 The invited lectures and presidential address delivered such fellowships will be awarded on 9 December to indi- at Cornell University during the ASA's 1962 annual viduals planning additional study or research for the pur- meeting appear in Special Publication No. 1, Food for pose of increasing competence in their own or related fields Peace, April 1963. Copies are available, as long as sup- of science. These fellowships, whose primary objective is plies last, from Matthias Stelly, Executive Secretary, to enable individuals several years past the doctoral degree American Society of Agronomy, at the above address. to supplement their training, will be awarded in the mathe- matical, physical, medical, biological, and engineering sciences, and others, and in certain interdisciplinary fields Graduate Studies in Agrometeorology such as oceanography, meteorology, biochemistry, bio- at Ontario Agricultural College physics, and geochemistry. Selection of fellows will be made by the Foundation Ontario Agricultural College, Guelph, Canada, invites from among citizens and nationals of the United States applications for graduate work in agrometeorology lead- on the basis of ability. Stipends are of the salary-match- ing to the M.S.A. degree. The program, under the di- ing type, based on the recipients salary income for the rection of an inter-departmental committee, offers an 1963-1964 academic year. Travel allowances may be opportunity for students to participate in one of several paid at the discretion of the Foundation. active research projects and to obtain courses required for specialization in this field. Applications for fellowships must be received in the Fellowships Section, Division of Scientific Personnel and Students will be required to complete a thesis based Education, National Science Foundation, Washington 25, on original research. Special emphasis is presently being D. C., not later than 7 October 1963. Application ma- given to studies of the microenvironment of field crops. terials may be obtained from the same address. Selections Research areas include a) The physical processes: radi- will be announced on 9 December 1963. ation and heat exchange, evapotranspiration, turbulent transport of carbon dioxide, etc.; b) The influence of at- (More ANNOUNCEMENTS on page 519)

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