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Aerobiology in plant pathology

J. M. Hirst
a a

The Cottage, Butcombe, Blagdon, Bristol, BS186XQ, England Published online: 01 Sep 2009.

To cite this article: J. M. Hirst (1991) Aerobiology in plant pathology, Grana, 30:1, 25-29, DOI: 10.1080/00173139109427765 To link to this article: http://dx.doi.org/10.1080/00173139109427765

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Grana 30: 25-29, 1991

Aerobiology in Plant Pathology

J. M. HIRST

Hirst, J. hl. 1991. Aerobiology in plant pathology. September 1991. ISSN 0017-3134.

- Grana 30: 25-29.

1991. Odense,

The Cottage, Biitcombe, Blagdon, Bristol BSI86XQ, England.

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The International Association for Aerobiology did me the unexpected honour of electing me an Honorary Member in 1986, but this is the first opportunity I have had to thank you publicly. The invitation to give this paper also presents me with a problem. For about 20 years I have done nothing in aerobiology until this year. Now I awaken as a Rip van Winkel, unwitting of most of what has transpired in that time and with material and illustrations equally dated. I can do no more than present aerobiology as I last saw it, to act as a yardstick against which to measure progress. I claim to be no prophet but I will also take a peep into the crystal ball of future possibilities. To keep anywhere near my alloted time I shall have to be selective. I shall omit all the important animal vector components o f aerobiology. I shall shamelessly concentrate on the mycological aspects but shall permit some wandering into the interplay of dispersal by air and water. I must consider:
What organisms are concerned, how to identify, enumerate, assess and predict thcir activity? When and how they occur, move, reach hosts, infect and survive and in what numbers? What the aerobiologist can do to help plant pathologists and farmers to assess, predict and decrease the effects of epidemic pathogens.

With that agenda it would be impossible to ignore the debt that I, aerobiology and plant pathology owe to Philip Gregory. Not only did he re-awaken microbial aerobiology but with the help of John Stedman he patiently established principles and a quantitative basis for particle dispersion and deposition on crops. They showed quantitatively how narrow obstacles exposed in fast winds are preferential deposition sites, how the orientation of surfaces and turbulent airflow modify deposition and how selective are

freely exposed sticky surfaces for the larger airborne particles. Gregory also delighted in putting to peaceful use the air samplers originally developed to sample poison gases. One of the most important of these was K. R. Mays excellent Cascade Impactor. The few original hand-made versions almost became articles o f veneration. The Cascade Impactor showed that many of the spores most important to plant pathology (and allergy) could be caught efficiently with only the second of its four impaction orifices. This enabled the development of the awkwardly named automatic volumetric spore traps, in which a slide was moved past the modified 2 x 14 mm orifice at 2mm per hour to permit discrimination of the time of capture. Not only did this reveal circadian rhythms and the responses to changing weather but it caught a much more representative sample of all but the smallest airborne particles and allowed their frequence t o be expressed in volumetric terms. In the 40 years since then the traps have undergone considerable improvement and manufacture and sometimes suffered crude copying. You can still find some of todays thousands of offspring on the trade stands at this Conference. Of course I am pleased they have lasted so long but it does seem surprising that they have not yet been replaced by better designs. What did it do and what would we have liked it to do? For general aerobiological surveys, as well as usually in plant pathology, a trap should deal equally with spores as different in mass as a large pollen, the range of fungus spores and the minute spores of actinomycetes. The previously used freely-exposed surface traps caught very few of the smaller spores and the efficiency of deposition of all was extremely variable depending on wind speed and was also affected by the size and orientation of the trap.
4th Inr. Con/.Aerobiol.lStockholmll990

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. I . hl. Hint

Particularly to the plant pathologist it was important to recognize the characteristic sporas of wet air or nightime as contrasted to the usually drier air by day. These rhythms and the changes brought about by weather gave the plant pathologist the means to study the pathogenic fungi in action and to start the clock on many infection processes. Later they proved useful to veterinary pathologists and allergists through being able to relate the onset of symptoms to the changing content of the air. The method had and retains enormous limitations, first of course its reliance on visual recognition. I commiserate with all the many here who have shared the tedium and eyestrain of scanning slides day after day. Experts do develop almost subconscious skills of spore recognition akin to those by which a shepherd recognizes each sheep in his flock. But with a complete reliance on visual recognition every count involves an act of faith and there are few clues as to whether any spore was alive or dead when caught. If it is the chemical composition of particles rather than their viability that defines allergenicity, then the allergist may be equally interested in particles alive or dead, as a fragment or even faeces. Botanists may need to know whether pollen is viable but this does not concern the fossil palynologist, because pollen grains may remain just as recognisable for millenia as on the day they were liberated. But, I shall stake my claim that among aerobiologists, the pathologists have the most difficult task and are perhaps still the least adequately served with techniques. Even if he was certain of identifying a spore and saying whether it was live or dead the mycologist would still be poorly equipped. For example, many fungi grow, disperse, fertilize or infect in very different life stages and apparently unrelated morphological forms. In recent years mycologists and specialists in spore identification have patiently made progress in spore recognition and in relating the perfect (sexual) spores of so-called imperfect fungi previously known only by their asexual spores (I make no apology for using ancient terminology because I think it is more intelligible to non-mycologists). Thus, recognizing that several of these very dissimilar spore forms may represent but one fungus is very important to the plant pathologists because some of the forms may occur only seasonally; perhaps serving as-survival forms during the absence of
4th Int. Con/. Aerobiol.lStockholmll590

hosts or unfavourable weather; others may be diplodizing forms effecting genetic recombination or be asexual spores capable of enormously rapid multiplication and causing epidemics. To complete the confusion, the spore forms may or may not be recognimble, may have different means of dispersal including water or insects, may infect othenvise quite unrelated hosts at different but quite essential stages of their life cycles and perhaps be able to infect only where the pathogens genetic constitution provides a capability to circumvent the resistance mechanisms that plant breeders have engineered into the changing spectrum of its host crops. Such duplicity and the ingenuity of dispersal mechanisms among fungi will come as no surprise to those familiar with the work of Terence Ingold or Don Meredith who showed how fungi have developed architecture or exploited so many physical processes to ensure that their propagules traverse the laminar air boundary layer around plant surfaces to reach turbulent air and experience all the joys and perils of dispersal. Often the discharge mechanism determines the diurnal periodicity or ensures that release coincides with conditions favouring infection. My cxperience suggests that there is often a much more refined mechanism underlying what may appear simple. While much effort and theorising has been devoted to the energetics of the drop secretion that accompanies the release of ballistospores, we know very little of the mechanisms that determine what seems to be the two stage process of disjunction of the conidia of cereal powdery mildew. Such processes can be very important epidemiologically for plant pathogens. Airborne sporangia of Pliytoplitliora infestam, the cause of potato late blight usually become prevalent in the air at about sunrise when drier air from above the crop begins to be mixed by turbulence with the humid air within the crop that would have been needed overnight to encourage sporulation. It is often stated that sporangia are stripped-off by wind or dislodged by the twisting of the sporangiophores. To a degree the latter is true but the requirements are precise. Sporangia are not released when sporangiophores are shaken by severe gusts of wind, nor when shrunken, dried sporangiophores are exposed to wet eddies. Most are dislodged only when fully turgid sporangiophores are exposed to brief dry air gusts. Then, I believe, the drying affects the delicate hygroscopic

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General Lectiire: Aerobiology in Plant Pathology

27

spiral wall structure more quickly than it can decrease the volume of the contained cytoplasm. So the pressure increase caused by the twisting, blows off the sporangium rather as would the cork in a water-filled plastic bottle be ejected if you trod on the bottle. This theory of sporangial liberation would agree with the usual microclimate at the time of increasing liberation but it might seem risky, almost suicidal, for a fungus known to be very sensitive to desiccation and to need wet leaf surfaces in order to infect. However, the speed with which it can defoliate a potato crop and the severity of the 19th century Irish Potato Famine leaves no doubt that it knows its business well. How does it manage? Studies of the birth of potato blight epidemics show two patterns of spread, one within plants and most densely for 1 or 2 metres around a source of infection usually depends on water dispersal, while air dispersal is the less frequent, more risky gamble by which distant crops may be infected by airborne spores finding wet conditions congenial for infection. Gregory and associates (Gregory et al. 1958) were the first to quantify the process of dispersal by rain splash, the optimum conditions, the effect of the size of the falling drop and its velocity on the number and trajectory of the many splash droplets resulting from the collision. Furthermore that the droplets could pick-up fungus spores from leaf water films. In crops both splash and air dispersal gradients will be influenced by wind. In an attempt to compare gradients generated simultaneously by the two processes, we used a dropping tower to aim and accelerate drops of water or fluorescent tracer (containing stained Lycopodiiim spores, 32 pm) to near terminal velocity before striking a splash target. Immediately beneath the splash target (0.5 m above ground) we released unstained Lycopodiiim spores into air. Assessments on the splashed tracer caught on horizontal surfaces along radii, showed that in still air almost all was within a circle of 1m radius, whereas in a wind of c 3m sec- tracer could be detected for at least 20m along the downwind radius. Being conducted in dry weather and mostly over short grass, the tests comparing wet and dry dispersal gradients must be admitted to be somewhat artificial because crop obstacles were not always im3

posed and washing or resuspension from second splash was prevented. The gradients of stained (splash-borne) or unstained (airborne) Lycopodium spores caught on horizontal slides or vertical cylinders near the source were markedly different. With the former, as expected being much steeper. There is need for much more of such information in different crops and weather and better means of determining where splash droplets dry so that hydrobiology becomes aerobiology. To serve agriculture, aerobiologists should understand deposition patterns within crops and from area- rather than point sources. It is important to know what proportion of spores (or pollen) released in a crop escape local deposition to introduce pathogens (or cause allergies) at a distance (or, conversely, what is the safe isolation distance from other crops to ensure that the efforts of breeders of hybrid crops are not frustrated by unwanted crosses). More recently, the request is to specify dispersal limits and conditions for the safe release of genetically engineered micro-organisms. Aerobiology was not equipped to answer such questions, so we began studying the fate of spore clouds generated by or arriving in crops of wheat or field beans (Vicia faba), both c lrn tall. W e had arrays of spore traps and meteorological instruments within the crops and up to 4m or 6 m a.g.1. At all heights we operated rotorod traps, together with sticky slides and cylinders within the crops. By following the spore cloud out of a source crop and into a sink crop we could demonstrate many of the complex processes at work. Studying the concentration (spores m-3 air) of various spores from source crops showed a rapid increase in the first few metres from the upwind crop edge, thereafter liberation was roughly balanced by depositjon within the crop but turbulent diffusion progressively increased concentration above the crop. Downwind of the 50m wide source crop turbulence very quickly decreased concentration near the ground, both by deposition and upward diffusion. When spore clouds from external area sources entered crops (e.g., sugar beet pollen entering crops of wheat or beans) the concentration was very rapidly decreased by deposition on crop surfaces. Just above the crop concentration was greater than within it, indicating a downward flux of spores into
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J. A!. Hirst
With the prevailing S W winds the air over Britain is commonly changed about twice a day; thus the intermittent sources of day and night spores often produce distinct alternating clouds down wind. During dry weather the base of all clouds bccome preferentially eroded by deposition as they cross unproductive land or sea. Within the limits of convection and turbulence the cloud continuously diffuses and settles. There is a suggestion that the heavier pollen grains sink more than the smaller spores.

the crop, but both upward and downward diffusion continued so that after l 0 m of travel the immigrant spores were barely detectable at all heights. I believe that all branches of aerobiology could profit from more factual data of this sort because there is now so much better capability to use it to model dispersion and deposition phenomena and with current meteorological knowledge to begin to estimate the escape fraction, to predict the depletion of the cloud by ground deposition or rain-washing during travel, and the patterns and magnitude of deposition and even look forward to estimating the magnitude of deposition in receptor crops. The greater the distances involved, the. more essential becomes collaboration with meteorologists both for detecting sources and understanding the processes of distant dispersal. By comparing the time of capture of exotic spores with regular trajectory analysis it is often possible to identify probable source areas. For example if spores of wheat rust coincide with air trajectories from western Europe but neither from the Atlantic, the North Sea nor eastern Europe then there is some evidence to presume possible sources. Experience also suggests that vertical spore profiles with their maximal concentration about a thousand metres above ground are often indicative of the preferential erosion (through deposition on land or water) of the base of a cloud that has travelled far. More recently much has been learnt by studies of the movement of pollutants and with viruses such as cattle foot and mouth disease has even reached a remarkable predictive capability. Advance in cases of botanical aerosols has been very restricted. Once airborne, spores behave exactly as the laws of physics and meteorologists say they should. Settling of,the cloud as a whole is presumably continuous but its effect is easily masked by wind, convective ascent, eddy diffusion, ground deposition and rain washing. Opportunities for detailed study are few but during one flight from the Humber to the Skaggerak (Hirst & Hurst 1967) we arranged for the aircraft of the RAF Meteorological Research Flight to collect triplet samples at regular interval between near sea level and about 3,000m during alternating gradual ascent and descent. Analysing this and other flights for concentrations of.Cladosporiiim, pollens .and damp air .fungi and relating them to trajectory analysis confirmed the following generalisations.
4Ih Inr. ConJ. Aerobiol.IStockholtnll990

If at its densest point the whole spore profile had been deposited by rain-wash, something like 10 spores would have been deposited all over Jutland. An impressive number but in plant pathological terms quite inconsequential until we can say how many remained infective. That brings me to my last, most important and most difficult subject, the recognition of identity, viability and functional capability. That favourite culture plot, the Petri dish provides room for but a very few fungal colonies to be grown to the size where they can be identified, there is a risk of adjacent colonies suffering from, overgrowth and mutual interference. Bacteriologists have managed better because their colonies are usually smaller, the organisms are more responsive to selective media and to serial dilution plating. Even so, in efficient samplers such as the Andersen Sampler or the Porton Impingers, bacteria and other organisms often suffer from overcrowding or damage through rough treatment. Throughout aerobiology there is therefore a great need for a new collector which is gentle, sterilizable, efficient over a wide range of particle size and capable of being operated for long periods without becoming oversaturated. The capability of diluting catches or splitting between a variety of culture media would be advantageous. Even such a utopian instrument would not satisfy the aerobiological plant pathologist who needs to determine the time, range and quantity of effective dispersal. Most parts of that brief statement present difficulty to the researcher, let alone to the practitioner but the most difficult probably lies in the one word effective because that implies the pathogen being productive, the host receptive and the time and weather propitious to the completion of the infection processes. Only then can the disease process be consummated. We know that distant travel can happen, that

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Geiieral Lecture: Aerobiology in Plant Pntliology

many organisms are very delicate but we have very little information about the reaction of plant pathogens to the hazards of desiccation, freezing, ultra violet radiation or airborne pollutants. Thus we cannot estimate the distance, extent, number or frequcnce of deposition of live spores. Were it not for their own form of beauty, the microfungi would b e unattractive and abominably difficult organisms with their changing forms, fickle and evanescent appearance, the difficulty of growing many, other than on hosts of specific genetic constitution, and the need of some, for very particular infection conditions. These complications I think create difficulties enough to defeat the everyday techniques of mycologists and pathologists. Do I see any hope? Yes, certainly in the extreme precision and sensitivity of the newer tcchniques of immunology and molecular biology. These must constitute the great hope and the current major challenge for aerobiologists. But they will I fear demand much revision of methods and may answer only extremely prccise questions rather than offer any easy panacea.

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REFERENCES
Gregory. P. H.. Guthrie, E. J. & Bunce, hl. E. 1958. Experiments on splash dispersal of fungus spores. - J. Gen. hlicrobiol. 20: 328-353. lint, J.hl. & Hurst, G.W. 1967. Long-distance spore transport. - In: Airborne Microbes. 17th Symp. SOC. Gen. hlicrobiol. (ed. P. H. Gregory & J. L. hlonteifh), pp. 307-344. - Cambridge Univ. Press, Cambridge.

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