Ecology and Epidemiology Relation Wear Variables and Periodicities Airborne Spores Aiternaria dauci W J Langenberg, J C Sutton, and T J Gillespie Former Graduate Student, Department Land Resource Science; Associate Pressor, Department Environmental Biology; and Associate Pressor, Department Land Resource Science, respectively, University Guelph, Guelph, Ontario, Canada NIG 2W1 Present address senior author, College Agricultural Technology, Kemptville, Ontario KOG 1J0 The authors thank staff Muck Research Station, Kettleby, Ontario, for assistance with field studies, Pesticides Advisory Committee Ontario Ministry Environment, and Ontario Ministry Agriculture and Food for financial support The assistance D J Hamilton in preparation figures is gratefully acknowledged Accepted for publication 5 January 1977 ABSTRACT LANGENBERG, W J, J C SUTTON, and T J GILLESPIE 1977 Relation wear variables and periodicities airborne spores Alternaria dauci Phytopathology 7: 879883 showed a characteristic circadian periodicity Few spores were dispersed at night when host leaves were wet, relative humidity (RH) high, temperatures cool, and wind speeds low Numbers spores increased after 0800 hours when leaves dried, RH decreased, and temperature and wind speed increased Peak populations occurred at about 1300 hr Prolonged high winds, periods rain or persistent leaf wetness, and cool temperatures during dew periods resulted in atypical periodicities and few airborne spores Limited amounts blighted leaves, low temperatures, and short dew periods were major factors restricting spore production Trends in wear variables, leaf blight, and numbers airborne spores Alternariadauci were monitored in carrot fieldplots during two growing seasons Wear factors during July frequently favored spore production, liberation, and dispersal, but low numbers airborne spores were detected because re was a scarcity sporebearing carrot leaves The numerous airborne spores which occurred during August coincided with periods favorable for spore production and release and increased blighting carrot leaves In September, low numbers airborne spores frequently were observed, usually after nights when temperatures were too low for abundant sporulation during period leaf wetness Numbers airborne spores Additional key words: epidemiology, Alternaria leaf blight carrot examining interrelationships certain wear variables that limit or promote A dauci spore production, liberation, and dispersal at various times during season Leaf blight produced by Alternaria dauci (Kfhn) Groves and Skolko is major foliar disease carrots (Daucus carota L var sativa DC) in HollandBradford Marsh, an area intensive carrot production in Ontario The disease is controlled by six to 10 fungicide applications to foliage in period from late July to late September when most blight occurs Development a scheme for improved timing fungicide applications () depended upon definition effects wear on development and dispersal airborne spores A dauci Even though airborne spores (conidia) are means spread pathogen and thus are important in development carrot leafblight epiphytotics, relationships A dauci spore production, liberation, and dispersal to wear have not been described previously However, effects wear factors on spore production and dispersal A solani Sorauer, A porri(ellis) Cif, and A alternatawere studied by Rotem (11), Meredith (8), and Pearson and Hall (10), respectively, In work presented here correlative field studies trends in wear variables, blight development, and numbers airborne spores provided a means for MATERIALS AND METHODS Copyright 1977 The American Phytopathological Society, 3340 Plots carrot cultivar Spartan Sweet, which is highly susceptible to Alternaria blight, were established at Muck Research Station, at Kettleby, Ontario, in 1973 and 1974 The Station is located near center HollandBradford Marsh The plots were arranged in a randomizedblock design, and separated by strips noncropped soil about 08 m in width Each plot comprised seven rows carrots 31 m in length and spaced 043 m apart Some plots in each block received fungicide sprays (), but blight assessments reported here were made in five replicate plots that were not sprayed The carrots were sown on 21 May 1973, and on 24 May 1974, and grown according to Ontario carrot production recommendations (9) Numbers airborne spores, blight severity, and various wear parameters were monitored continuously from 25 June to 4 October in 1973, and from 21 June to 4 October in 1974 The incidence airborne spores A dauci above Pilot Knob Road, St Paul, MN 55121 All rights reserved, carrot plots was measured with volumetric spore traps In 879
880 PHYTOPATHOLOGY [Vol 7 1973, spores were collected with a Hirst automatic August until harvest time At each time assessment, 20 volumetric spore trap (C F Casella and Co Ltd, randomly selected plants in three center rows each London, England) which was placed with intake plot were examined On each plant, blight symptoms were orifice 5 m above ground level In 1974, spores were trapped with a Burkard volumetric trap (Burkard 80 Scientific Sales Ltd, Rickmansworth, England) located 0, 05 m above ground Alternaria dauci spores recovered in traps were ( 0 o identified according to criteria Ellis (1), counted, _ and numbers spores per cubic meter air were m / estimated according to Hirst (3) Because no corrections 40 / 9 973 were made for variation in trapping efficiency associated with wind speed, spore concentrations recorded are xe / underestimates true values Alternaria dauci spores LL 20 are morphologically similar to those A solani Sorauer wu and A porri (Ellis) Cif which also occur in Ontario j 1974 During 1973 and 1974, however, re were few hosts 0 20 30 10 20 30 A solani within 40 kilometers traps, and no purple AUGUST SEPTEMBER blotch disease produced by A porri was found or DATE reported in onions grown in HollandBradford DATE Marsh Thus, it was assumed that few conidia A solani Fig 2 Development Alternaria blight in field plots or A porri were present that could have been trapped and nonsprayed carrots in 1973 and 1974 confused with those A dauci Blight was assessed according to criteria Horsfall and Barratt (5) at intervals 7 to 10 days from early t:go H 90O ' 2505 t15 200, 0 50 W 0J z 100I 1 I i I I I_1 ii i_ 80 WET DA T IN 19S 40 00 14 22 2 312 0 14 22 2 312 1O 14 12 22 2 30 0 30 2: 20 IF 100 0200 80 4 JULY AUGUST SEPTEMBER OCT'I 0 1'I'I'I'I 1 ' I ' ' w DATE IN 1973 40 2n 0i21 2 22 cn0 100 awn in 40 2E3 (ESTR IE TOLGT ý'no DATA M 0 PR 14 222 312 10 14 22 22312 10 14 22 23023 0l JULY AUGUST SEPTEMBER OCT 01 41 82 22 DATE IN 1974 2481 41 82 2ý Fig 1 Cummulative daily concentrations airborne (EASTERN DAYLIGHT TIME) Alternaria dauci spores from midjuly to October in 1973 and 1974 The cumulative daily spore concentration equals Fig 3 Mean circadian trends airborne Alternaria dauci hourly numbers spores recovered per cubic meter air spores, air temperature, relative humidity (RH), occurrence arithmetically summed during respective 24hr period, leaf wetness, and wind speed for July to 3 October 1974
July 1977] LANGENBERG ET AL: ALTERNARIA SPORE DISPERSION estimated in four expanded leaves, one each from bottom, lowercenter, uppercenter, and top canopy Temperatures and relative humidities (RH) in carrot plots were measured with a hygrormograph (Lambrecht, Gttingen, Germany) located in a Stevenson Screen (instrument shelter) at 05 m above ground level in carrot plot and 10 m from spore trap Wind speed was monitored with a cup anemometer (Casella, London, England) mounted 5 m above ground level and 100 m from spore trap The duration leaf wetness was recorded with a DeWit leafwetness recorder (DeWit, Hengelo, The Nerlands) placed 05 m above ground level at 5 m from spore trap Sunshine was monitored with a 7day pyranograph (Wearmeasure, Sacramento, CA 95841 Solar energy data, as recorded by pyranograph, were expressed as precent each hour with "bright sunshine" using a conversion factor determined by simultaneous comparison with a CampbellStokes recorder (Casella, London, England) during a few selected days Precipitation was measured with a standard Atmospheric Environment Service Canada rain gauge 881 nearby carrot fields were very low during se periods The limited amount blighted tissue was probably due to scarcity inoculum and substantial resistance young carrots to lesion development (13) The moderatetolarge numbers spores trapped in periods 3 August to 15 September in 1973, and 27 July to 19 August and 8 to 15 September in 1974 coincided with frequent periods favorable for spore production and release and presence increasing amounts blighted carrot tissues (Fig 1 and 2) Low numbers airborne spores in September were observed on days following nights with temperatures too low for abundant sporulation during periods leaf wetness In 1973, night temperatures during to 23 September fell below 11 C, except on 22 September In 1974, night temperatures dropped below 11 C during 1st week September and ground frost occurred frequently after 15 September There were few airborne spores on days following nights with low temperatures even though conditions favorable for spore release were frequent Many spores were trapped on most days that followed nights with temperatures that favored spore production Mean circadian trends in numbers airborne spores Alternaria dauci and wear variables during 1974Mean circadian trends in airborne populations Seasonal trends in numbers airborne spores Alternaria dauciestimated numbers A dauci spores in air over carrot plots were expressed as cumulative daily spore concentration (CDSC), which equals hourly numbers spores per cubic meter air arithmetically summed during each 24hr period In 1973, mean CDSC was low (six spores) in period from 1 July (when first A dauci spore was trapped) to 2 August, moderate (52 spores) 310 August, and high (140 spores) 11 August to 15 September Peak CDSC values were 41 and 475 on 11 August and 15 September, respectively (Fig 1) In 1974, greater numbers spores were trapped than in 1973, but trap was located closer to carrot canopy A single A dauci spore was trapped on 21 June The mean CDSC was low (10 spores) until 27 July, n increased sharply, and remained high (51 spores) until 19 August In September, spores were scarce (17, 15, and 9 spores) during 1st, 3rd, and 4th wk, respectively, but were more numerous (103 spores) throughout 2nd wk (Fig 1) The seasonal trends in populations airborne A dauci spores were correlated with wear variables and blight severity Conditions favorable for sporulation A dauci are darkness, a leaf wetness duration at least 10 hr, and temperatures ranging from 11 to 23 C () A rough indication amount sporebearing tissue is given by percentage leaf area blighted (Fig 2) In 1973 and 1974, low numbers airborne spores trapped during early part growing season were (before 2 August and 27 July, respectively) tissues, host sporebearing scarcity a with associated but not with wear unfavorable for sporulation In 1973, wear favorable for sporulation occurred on seven nights between 1 July and 2 August, and in 1974 re were four favorable periods between July and 27 July Amounts blighted leaf tissues in plots and >_ 3,, 70 " X Jo %, "' 1iooz :) 't, 8_0 ",, 400S _r 320 2 sp,qeo % AV,," o 10 o 3 > 801, II"Z 2 JULY 27 2 JULY 28 2 JULY 29 (EASTERN DAYLIGHT TIME) Fig 4 Circadian periodicities in numbers airborne spores Alternariadauciin relation to wind speed, leaf wetness duration, sunshine, air temperature, and relative humidity during 27 to 29 July 1974
PHYTOPATHOLOGY 882 [Vol 7 hour occurred when leaves dried, RH declined, and temperature and wind speed increased Thus, release A dauci spores was correlated with a warming trend, increased air circulation, and consequential drying leaf surfaces and decrease in RH ambient air Peak populations airborne spores occurred about 3 hr before maximum wind speed, 2 hr before highest temperature, and 1 hr before lowest RH The decline in numbers airborne spores after 1500 hours did not coincide with changes in trends wear parameters; thus it possibly was related to a progressive depletion mature spores available for dispersal from carrot leaves Depletion spore supply by prolonged high wind speedson days 27, 28, and 29 July 1974, moderatetostrong winds (>5 m sec') occurred for periods 7, 8, and 5 hr duration, respectively, but airborne spores were numerous for 10, 5, and 0 hr during se respective windy periods (Fig 4) On 28 July, concentrations airborne spores increased sharply at 1000 hours, immediately after an increase in wind speed, but decreased sharply after 1300 hours, even though moderatetostrong winds persisted until 1900 hours During peak hours spore dispersal and strong winds, mature and immature spores and conidiophore fragments were recovered in spore trap Evidently source spores on carrot leaves virtually was depleted at 1500 hours Because average Stemperature 111 C observed during dew period 30 2728 July was at lower limit for abundant sporulation, (), even though temperatures during previous night 220 t were 5 C warmer, spores available for dispersal on 28 July wi probably were fewer than on 27 July On 29 July, even though conditions favored spore formation and subsequent spore release, few spores were which probably was related to a scarcity airborne mature spores on carrot leaves Conidiophore fragments trapped on 28 July indicated extensive destruction conidiophores by strong winds which would necessitate conidiophore regeneration before E spores could be formed The length time favorable for z sporulation in early hours 29 July may have been 0:o insufficient for formation both conidiophores and 10 "o_spores This is substantiated by occurrence 1L numerous airborne spores on 30 July, following anor period favorable for sporulation Suppression airborne spore concentrations during 0periods rain or persistent leaf wetnessnumbers airborne spores declined precipitously during a rain shower (2 mm) 30 min duration on 30 July 1974 (Fig 5) Spore numbers per cubic meter air in hours 3 > V\ I preceding, during, and following hour within which rain occurred were 350, 75, and 0, respectively A dauci spores in spore trap ceased abruptly just after rain began A dauci spores and wear variables were determined for 5day period from July to 3 October, exclusive 20 to 30 August when no spore counts were made For each day, hourly numbers spores per cubic meter air were normalized as a percentage maximum trapped during any hour that day Hourly values for temperature, wind speeds, RH, and occurrence leaf wetness also were recorded For each hour day, normalized numbers spores and wear data were averaged over 5day period and represented by circadian periodic curves (Fig 3) Concentrations airborne spores showed a marked circadian periodicity (Fig 3) Numbers spores were low from about 2200 hours to 0800 hours, n increased abruptly to maximum concentrations between 1300 and 1500 hours, and steadily declined reafter Similar circadian periodicities in airborne spore concentrations have been shown for A solaniand A tenuis (11), for A porri (8), and for A alternata(10) The circadian periodicity in concentrations airborne spores showed correlations with circadian trends in wear variables (Fig 3) During night and early morning, when numbers airborne spores were quite low, host leaves were wet, atmospheric RH high, temperatures cool, and wind speeds low The sharp increases in numbers airborne spores after 0800 > 1I00 (RH >_ 80 V EMP S0 It" 1 0 Z 50 0_ :'930 280" SPO7 /5 200 \ 10WINC 1200 40 U, orecovery 12 12 (EASTERN DAYLIGHTO E) (EASTERN DAYLIGHT TIME) 12 Fig 5Circadian periodicities in numbers airborne spores Alternariadauciinrelation to wind speed, leaf wetness duration, rain, sunshine, air temperature, and relative humidity on 30 July, 2 August, and September 1974 On night 1to 2 August 1974, conditions favored spore production, but re were few airborne spores following day On 2 August, warm and moderate winds developed However, because early morning cloudiness and afternoon rain showers, leaves were dry for only 4 hr Airborne spore populations declined abruptly after heaviest afternoon shower In se examples it is likely that both removal
July 1977] LANGENBERG ET AL: ALTERNARIA SPORE DISPERSION 883 airborne spores by rain and restriction spore reported frequently (2, 4, 8, 11, 12) Limited amounts blighted leaves, low temperatures, liberation by moisture on leaves contributed to and short dew periods were major factors restricting observed decreases spore concentrations Suppression numbers airborne spores on days production A dauci spores on carrot leaves, whereas following cool nightswind and dry periods favorable numbers airborne spores also were limited by rain or for spore liberation and dispersal occurred on several prolonged leaf wetness Low numbers airborne spores days after 15 September, including September (Fig 5), during July and September generally were associated but airborne conidia were scarce However, temperatures with restricted sporulation attributable to scarcity on preceding nights were too low for abundant blighted leaves and low temperatures On occasional days sporulation; thus, scarcity fresh spores is presumed to throughout season, periods leaf wetness were too short for spores to form On certain days, however, have limited airborne spore concentrations Integrated effects wear and host factors on prolonged or intermittent periods leaf wetness concentrations airborne sporesmoisture regimes restricted spore release Rain probably decreased exerted a major influence on concentrations airborne numbers airborne spores both by prolonging leaf A dauci conidia Absence or scarcity airborne spores wetness and by direct removal spores from air when leaf surfaces were wet indicated that surface LITERATURE CITED moisture prevented spore liberation However, amount surface moisture required to prevent spore 1 ELLIS, M B 1971 Dematiaceous hyphomycetes release is not known The abrupt increases in airborne Commonwealth Mycological Institute, Kew, Surrey, spore concentrations coincident with drying leaves England 08 p demonstrated importance dry leaf surfaces for 2 GREGORY, P H 1973 Microbiology atmosphere abundant liberation spores The liberation spores as p 377trap England Aylesbury, spore volumetric automatic Leonard An Hill, J M 1952 3HIRST, ecrasig aposibl eclnedindcatd ~2nd edition RH effect decreasing a possible efect indicated RH declined 39:25725 Bio2 A Ann in liberation Spore mechanism Appl Biol 39:25725 RH on sporerelease durng orml wathr b RHAnn ducimaybe Arigere 4 HIRST, J M 1953 Changes in atmospheric spore content: A dauci may be triggered during normal wear by RH diurnal periodicity and effects wear Trans Br declining from nearsaturation and may involve a violentmycol Soc 3:375393 release mechanism similar to that reported by Leach (7) 5 HORSFALL, J G, and R W BARRATT 1945 An for Alternariatenuis and or porosporous fungi, and by improved grading system for measuring plant diseases Meredith for A porri (8) Phytopathology 35:55 (Abstr) Peak concentrations airborne conidia A dauci W J 1975 Carrot leaf blight (Alternaria LANGENBERG, solaniin A for peaks but sunrise, after hr 5 occurred in relation to environmental factors development dauci) to (11) Rotem Negev Desert Israel were found by and fungicide applications MSc Thesis, University Canada 119 p Ontario, Guelph, Guelph, peak earlier occur only 45 hr after sunrise The 7 LEACH, C M 1975 Influence relative humidity and redconcentration for A solani may be related to earlier and infrared radiation on violent spore release by Drechslera more rapid drying in Negev than occurred at turcica and or fungi Phytopathology 5:13031312 HollandBradford Marsh Rotem postulated that early 8 MEREDITH, D S 19 Spore dispersal in Alternaria porri drying hastens peak hour spore dispersal (Ellis) Cif on onions in Nebraska Ann Appl Biol 57:7Wind is required for dispersion spores (2), but its role 73 in ir detachment from conidiophores is not known 9 ONTARIO MINISTRY OF AGRICULTURE AND The liberation both mature and immature spores and FOOD 1973 Vegetable production recommendations conidiophore fragments during prolonged periods Ministry Agriculture and Food, (Canada) Ontario 33 4 p Publication strong winds indicated that wind may enhance spore liberation temporarily However, decreasing numbers 10 PEARSON, R C, and D H HALL 1975 Factors affecting occurrence and severity black mold ripe tomato airborne spores on successive days when strong winds fruit caused by Alternaria alternata Phytopathology occurred, and frequent occurrence peak numbers 5:13521359 airborne spores for several hours before a decline in wind speed (Fig 4), indicated that strong winds may result in 11 ROTEM, J 194 The effect wear on dispersal Alternaria spores in a semiarid region Israel depletion spores available for liberation from leaves, Phytopathology 54:2832 reduce wind which was reported by Rotem (11) Gusts P E, and J G HORSFALL 199 Epidem WAGGONER, 12 surrounding air still layer boundary thickness A simulation plant disease written for a computer Conn Agric Exp Stn Bull 98 80 p leaf surface, reby exposing more spores to action wind eddies The increased movement and 13 ZIMMER, R C 197 Carrot blight in southwestern Ontario and importance radiation and temperature mutual abrasion carrot leaves that occurs with in sporulation Alternaria dauci PhD Thesis, increased wind speeds may encourage dislodgement A University Western Ontario, London, Ontario, dauci spores into turbulent air Increases in numbers Canada 9 p airborne spores with accelerated wind speeds have been