Bacterial flux from chaparral into the atmosphere in mid-summer at a high desert location

Pergamon

Atmosphrrtc Enstronmenr Vol. 28, No 1, DD 1267 1274. 1994

1X2-2310/94 S6.00+0.00

1352-2310(94)EOOlO-H

BACTERIAL ATMOSPHERE

FLUX FROM CHAPARRAL INTO THE IN MID-SUMMER AT A HIGH DESERT LOCATION B. LIGHTHART

U.S. Environmental

Protection

Agency.

Environmental

Research

Laboratory,

Corvallis,

Oregon,

U.S.A.

and B. ManTech

Environmental (First

Abstract-Estimates

Technology,

rrcriord

25 Auyust

T. SHAFFER

Inc.,

200 SW 35th

Street,

1993

and injnalform

13

Corvallis,

OR 97333,

U.S.A.

December 1993)

of the bacterial flux for a daylight cycle were observed at the Hanford Nuclear

Reservation. Richland, WA. during June 1992, using a modified Bowen ratio method. The upward daytime bacterial flux was coupled with the solar radiation/sensible heat cycle, but commenced 2 h later in the morning and ceased 3 h earlier in the afternoon. During this period, the maximum flux was cn. 17,000 Colony Forming Units (CFU) rnmr h- ’ occurring at solar noon, resulting in a total upward bacterial flux of co. 76,000 CFU m - * for the time period. During this same period, the integrated total viable bacterial concentration in the atmosphere was only 0.81% of total upward bacterial flux. The high temperatures (e.g. 45 C). low relative humidity (e.g. IO%), and particularly high solar radiation (e.g. 910 W m-‘) are thought to be the lethal agents in the high desert atmosphere. The decreasing concentration ol bacteria in the atmosphere was found to slow within 30 min of the initiation of the upward flux of bacteria. Even though the upward flux of bacteria decreased after solar noon, the bacterial concentration in the atmosphere continued to increase. Presumably, this is due to reduced solar radiation in the afternoon allowing greater survival of the released bacteria and smaller dilution of entering bacteria into the shallow nocturnal mixed layer. Key

word ir1dr.v: Bioaerosol,

model.

vegetation,

release

1973) and dilution effects due to atmospheric layer events (Stull, 1988; Frisch et al., 1990).

INTRODUCTION The transient concentration of outdoor atmospheric bacteria (F&on, 1966a. b; Fulton and Mitchell, 1966; Kelly and Pady, 1954; Pady and Kramer, 1967) is the

temperature

(Dimmick

and

Akers,

1969;

mixed

Theoretical

result of a dynamic equilibrium between the bacterial input and output fluxes* to and from the atmosphere. In the unobstructed high desert at the Hanford Nuclear Reservation at Richland, WA, in mid-summer, the input flux is primarily from the chaparral and soil, while the output flux depends upon non-conservative properties of the bacteria. Some of these properties include damaging and lethal effects of solar radiation (Sharp, 1940; Harm, 1969; Lighthart and Shaffer, unpublished data), de- and re-hydration of bacterial cells (e.g. Crowe er cl/.. 1990: Israeli et ul.. 1993) and extreme

rate, micro-organisms.

Cox,

1987) effects, as well as certain physical and meteorological factors such as gravitational settling (Gregory, l Bacterial flux is defined as number of colony forming units (CFU) passing perpendicularly through a unit area in a unit time, e.g. CFU m ’ h ‘.

1267

The concentration of viable airborne bacteria ([Blair; colony forming units (CFU) m- 3, is the difference between the input flux (ki; CFU m-‘h-l) to the atmosphere from some source (Bacteria,,,,,,) and output flux (k,) from the atmosphere to some sink(s). This dynamic equilibrium is defined for some time interval (At) and mixed layer (ML) depth (zi) in equation (1). A[Blai, -= At

bacterial

(input

flux-output

flux)

mixed layer depth ki-k, zi

(1)

The keystone to evaluating the dynamics of the airborne bacteria is measuring their input flux. For outdoor sources, the input flux may be primarily from vegetation, as seen by Lindemann et al. (1982) where they found up to 543 CFU m-‘s-’ (or 1,954,800

1268

B. LIGHTHART

and B. T. SHAFFER

CFUm-2h-‘)fromcropsand 124CFUm-‘s-‘(or 446,400 CFU mm2 h-‘) from thesoil surface. The Bowen ratio method (Stull. 1988; Huebert and Robert, 1985; Huebert et al., 1988) has been called the present-day method of choice to estimate the near surface flux of bacteria from the ground into the atmosphere (J. Businger. pers. comm.). The method is based on the ratio of the sensible heat flux (bv’r’) and heat difference (AT) at two heights above ground level (a.g.l.), to the bacterial flux (ki) and bacterial difference (A[bacteria]) at the same two heights (equations (2) and (2a)). Bacterial flux Sensible heat flux = Bacterial difference Temperature difference or more explicitly,

solving for the bacterial

(‘1

flux

(24 The sensible heat flux may be computed by subtracting a 200-s running mean from the instantaneous temperature (T’) and vertical wind speed (w’). and averaging their products over each l-h bacterial sampling period (Huebert and Robert. 1985; Huebert rf al. 1988). The air density (p) and specific heat (C,) used in Huebert and Robert (1985) and Huebert et al.. (1988) are included in the National Center ~-~ for Atmospheric Research (NCAR) measurement of &T’ used herein. The downward direction of sensible heat flux is negative by convention and the units are in W m-‘. Therefore, if the flux out the top of the ML is assumed nil (i.e. zO), and both horizontal and vertical mixing results in relatively homogenous ML concentration, then in the first approximation of atmospheric bacterial dynamics. the concentration of bacteria in the ML could be a function of the residual bacteria from the previous day, the input bacterial flux. lethal or damaging meteorological factors of solar radiation (SR), atmospheric moisture and temperature, and the ML depth. Purpose

In the future, there is a potential for anthropogenic microbial air pollution (MAP) associated with largescale use of microbial pesticides (Flexner er al., 1986; Miller, 1990) and other microbials in forestry and agriculture, and other agricultural practices (Lighthart, 1984) and urban activities, particularly sewage treatment and solid waste composting (Anonymous, 1991). If we are to manage the atmospheric bacterial loading from these sources. we must have a better understanding of the dynamics of airborne bacterial populations. This report describes a first step in understanding these dynamics by evaluating the flux of bacteria during daylight hours at an isolated location in the high desert chaparral. The idea here is to use the flux of bacteria from natural sources as a surrogate for micro-organisms applied to vegetation by man.

METHOD

The observations were made from 4 to 8 June and 24-27 June, 1992. at the Hanford Nuclear Reservation. Richland, WA (~a. 600m elevation), in conjunction with a micrometeorological source FOOTPRINT92 study conducted by Washington State University and University of Quebec at Montreal with cooperation from the National Center for Atmospheric Research (NCAR) (LeClerc PI al., 1992). The experimental site was flat. with an infrequently used highway approximately 300 m to the south and one-storey buildings approximately 900 m lo the west.t The prevailing winds were from the west. The vegetation at the site consisted of sagebrush and grasses. The atmosphere was very clear during the observations. Merroroloyicul A IO-m meteorological tower (Campbell Scientific Inc., Logan, UT): was modified (0 support both meteorological sampling devices and a specially designed bacteriological sampler suspension system (Fig. I). The meteorological instrumentation consisted of temperature sensors (Campbell Scientific Inc.. Logan, UT) located on the tower at 2. 4. and 8 m a.g.1.. hygrometer at 4 m a.g.1. (Campbell Scientific Inc., Logan. UT), and pyranometer (LI-COR. Inc.. Lincoln, NE), cup anemometer. and wind direction (Met One, Inc., Grants Pass. OR) at 10 m a.g.1. All sensors were located so they had at least a I20 upwind acceptance angle. Measurements for IV’T’ and :,‘L (i.e. :/L=(. and is a measure of mechanical and’or convective turbulence) were made at one of NCAR’s meteorological array towers (Businger YI ul., 1990) approximately 30 m from the bacterial sampling tower. Bacteriolayical The bacteriological sampler suspension system had three sampler support platforms hanging sequentially from the top of the tower by stainless steel cable attached at each of their four corners (Fig. I). The platforms were 2, 4 and 8 m a.g.1. and held either two Andersen 6-stage cascade impact samplers (Andersen Instruments Inc.. Atlanta, GA) or two slit impact samplers (S-T-A Biological Air Sampler. New Brunswick Scientific Co., Inc., Edison, NJ). or one of each (Wolf et (I/.. 1964). Samplers were run for I h at an inflow rate of 28.3 / min ‘. The platforms were lowered and raised with a hand winch located at the base of the tower. A vacuum line for the samplers on each platform was tied to one of the platform suspension cables while the electrical power cable was self-hanging from each platform. All bacterial samples collected were impacted onto Luria Bertani agar (LB; Difco Laboratories, Detroit, MI) and then incubated for 7 d at 25°C. Ten-second “control” samples were taken before and after each observation period to evaluate the potential for contamination of the sterile agar impaction plate during its placement in the sampler and sampler startup procedures. Analytical Curvilinear regressions, their confidence intervals, polynomial equations. coefficients. and coefficients of determination (R’) for the airborne bacterial concentration, bacterial flux. and solar radiation were computed using SigmaPlot” \‘1 I I.I.G~!,I Sclcnlilic. Cortc Ma&r.,. CA). Mathcmarical determinations of polynomial derivatives, their maxima and

t The “rule of thumb” states: to negate any turbulence erects of an upwind obstacle, multiply the sample height in

meters by 100 to get Ihe required uniform fetch in meters. 2 Mention of trade names or commercial products does not constitute endorsement or recommendation for use by the Environmental Protection Agency.

Bacterial

Ughtsnlng cup

rod.

anemometer

flux

1269 ‘.

.....................

Pyranometer

.................... Wind

direction

Sampler-suspension pulley rod Slit sampler

Andersen

Platform pulley

sampler

suspension rope

Sampler platform support wires Temperature/ hygrometer

D I I.....

Hand

winch’

.’

Data

logger

.......

........

‘.

Electrical Sampler

J

Ground

showing

arrangement of meteorological and bacteriological above ground level on the 10 m meteorological

minima, inflection points, and integrations were done using Mathmaticc9 (Wolfram Research, Evanston, IL). Least-squares regression polynomial models, using powers of time as the covariates, were fit 10 the bacterial concentration and flux, temperature, relative humidity (RH), sensible heat flux (w’T’) and Z/L (i.e. zeta or C,) data to determine the lowest order model that adequately fit the data (see Appendix). Higher than fifth order models resulted in biased coefficients due to their linear dependences on the covariates.

wire

Vacuum hose to each sampler platform platform suspender anchor

.._._..........__.......

I. Diagram

platform

.......

Electrical

Fig,

connector

instrumentation tower.

at 2, 4, and 8 m

The third, fourth, and fifth order models were selected since all covariates (i.e. lesser order time terms) were statistically significant (p CO.01) in all cases. RESULTS

Although there was a relatively high variability in the hourly bacterial counts in the atmosphere as seen

1270

B. LIGHTHART

and B. T. SHAFFER

4

Time of day (24 hr clocW100) Fig. 2. Concentration of airborne bacteria at 2 m (L), 4 m (M), and 8 m (H) platforms above ground level, and for orientation, solar radiation during the observation periods at the Hanford Nuclear Reservation. Richland, WA. The fourth order curvilinear regression line and 95% confidence limits arc the means for all samples. The solar radiation curve shown in all figures is for orientation purposes.

in the scatter of the data shown for the three sampling heights in Fig. 2, fourth order polynomial curves (not shown) described their concentration with time trends rather well, as indicated by their coefficients of determination (R’), which were 0.75, 0.64 and 0.71 for the high, middle and low platforms, respectively. The mean bacterial concentration of all sampling platforms during the sampling period (i.e. Mnthematica’s fourth order polynomial fit line in Fig. 2) decreased from an early morning (ca. 0600 h)t high of ca. 109 CFU mm3 through an inflection point at ca. 0955 h to a minimum in the early afternoon (ca. 1320 h) of 73 CFU m-3 and thereafter increased dramatically into the early night (ca. 2200 h) to ca. 275 CFU rnm3. The mean bacterial flux (Fig. 3) starting after ca. 0950 h was upward, reached a maximum of ca. 16,794 CFU me2 h-’ (or 16,794/3600=4.67 CFU m-‘s-l) at ca. 1325 h and decreased to nil or negative by ca. 1713 h. The total input of bacteria during this period (i.e. 0950-1713 h) was calculated to be ca. 76,050 CFU m-‘. The initiation of the upward flux of bacteria and the inflection-point time going from an increasingly to a decreasingly lower rate of change in the bacteria1 concentration was calculated to be within 5 min of each other, i.e. 0950 and 0955 h while the maximum flux and minimum count were within 5 min of each other, i.e. 1325 and 1322 h, respectively. During this positive flux period, the integrated number of t All clock

times

expressed

in Pacific

daylight

time.

bacteria found in a cubic meter of air was 612 CFU (Fig. 2). Assuming the ambient bacterial concentration measured by our samples was near a dynamic equilibrium between the influx and loss mechanisms, the ambient total population of bacteria in the air during the upward daytime flux period represented ca. 0.81% (=612*100/76050) of the total bacterial flux. Meteorological measurements showed solar radiation dawn and dusk at ca. 0425 and 2041 h, respectively, with maximum radiation of 908 W m-’ at 1231 h; solar heating of the ground resulted in the upward sensible heat flux (Fig. 4) commencing at ca. 0640 h, reaching a maximum at 1335 h of ca. 247 W m-‘, and thereafter declining to a neutral or negative flux by 2010 h; and both temperature and RH (Fig. 5) rapidly reaching the inverse of each of their daytime extremes of ca. 32’C at 1655 h and minimum RH of 9.6% at 1552, respectively; and thereafter relatively slowly returning to dawn levels. The atmospheric turbulence structure during the day (Fig. 4) as indicated by z/L, tended to be more convectively driven in the morning to ca. 1100 h, and more mechanically driven after ca. 1600 h in the late afternoon. DISCUSSION

The concentration of airborne viable bacteria in any particular atmospheric volume is thought to be a dynamic equilibrium between input flux from source(s) and output flux to sink(s). In the case of the

Bacterial

flux

1271

'\ ,~,',',-I'I'I'I'I

-40000 4

6

O

. _'

6

10

12

14

16

16

20

22

Time of day (24 h clocW1OO) Fig. 3. Mean hourly bacterial flux (circles) during daylight hours during the observation periods at the Hanford Nuclear Reservation, Richland, WA. Curve was generated by a least-squares fit of polynomial equations of the observations. The narrow lines above and below the bacterial flux are 95% confidence limits.

400

._.-._.._-r -------------,---I*----------___ i .!-w .’ \ . /l

0.0 -

-0.5 E 6 -1’ -1.0 g -1.5

-

E a9 300 Ff “K .” p! 2.E 200 5 C E 0 E 5 s

100

in o-2.0

0-1

0

I

o\

'\ r'1'1'1'I'I~I'I' 4 6

0

\: 8

10

12

14

16

1.9

20

22

Time of day (24 hr clock/l 00) . (-) conveci!ve (heal) turbulence / mechanical nubulenco (adapted lrom NCAA data)

(wind)

Fig. 4. Graph of mean hourly sensible heat flux (circles) and z/L, a ratio driven turbulence, during the observation periods at the Hanford Richland, WA. Both sets of values were adapted from NCAR

Hanford site, there were only two apparent local sources within 30 km of the observation tower: the epiphytic bacteria on the chaparral and soil surface. The sinks include dilution in the mixed layer, depos-

of heat-driven to windNuclear Reservation, observations.

ition and impaction, and aerial death of the cells due to solar radiation, high temperatures, and low relative humidity (Sharp, 1940; Webb, 1961; Harm, 1969; Webb and Lorenz, 1970; Pollard, 1974).

B. LIGHTHART

1272 2

B. T. SHAFFER

and

1000

35 7

Solar radmtion. R’.0.96

I -

3Ql

4

Temperature;

‘\

6

8

10

12

14

RL070

16

18

t

20

22

Time of day (24 hr clock/l 00) Fig. 5. Mean hourly meteorological conditions of temperature. solar radiation during the observation periods at the Hanford Richland. WA.

The chronological series of measurements made at the Hanford Nuclear Reservation indicate that the changes in the airborne bacterial concentration during daylight hours is the result of a series of events initiated with solar heating of the ground and leaf surfaces, resulting in a turbulent micro-layer gradient (see Stull, 1988, p. 252 for definition) that might cause the release of single and multiple bacteria, and particles with adhering bacteria (e.g. Lighthart et al., 1994) into the atmosphere. At the high desert sampling location, it was approximately 2 h after initiation of the upward sensible heat flux before the upward bacterial flux was observed. Prior to initiation of the upward bacterial flux, the concentration of bacteria was decreasing. Subsequent to initiation of the upward bacterial flux, the bacterial concentration continued to decrease but at a slower rate until solar noon, when the concentration was at its minimum. At solar noon the concentration started to increase in the presence of two competing processes: populationdecreasing lethal effects of SR, and perhaps increasing temperature and decreasing RH: and populationincreasing effects of the positive bacterial flux that reached its maximum about solar noon. After the Sun passed its zenith the solar radiation decreased, causing the sensible heat flux to diminish with a consequent decrease in the bacterial flux. One would have expected the airborne population of bacteria to also decrease at this time. This did not happen. The population increased after the solar noon. It is hypothesized that because the temperature and RH changed very little from their solar noon values (i.e. extreme daily measurements) while the SR did; the

relative humidity. and Nuclear Reservation.

decreasing SR allowed more of the newly released bacteria from the vegetation and soil to survive in the atmosphere. The large variation in midday bacterial flux is presumably due to upward directed convection and downward directed subsidence cells at the sampling

location

during

the time

interval

represented

by

the data points. Thus, before the solar zenith, bacteriareleasing processes are slightly greater than the removal processes (i.e. k,
even

though

the

bacterial

releasing

process

is

reduced, the removal processes are greatly diminished, resulting in an overall increase in airborne bacterial concentration in the afternoon and evening (i.e. k, >k,). SR may cause permanent or temporary lethal damage in airborne bacteria (Sharp, 1940; Webb, 1961; Webb and Lorenz, 1970; Pollard, 1974). Repair of temporary lethal SR damage may be activated either by longer wavelengths of light (so-called photoreactivation repair (Jagger, 1983)), beyond the damaging wavelengths, or spontaneously in the dark (so-called dark repair (Freifelder, 1987)). Thus in late afternoon and after sunset, photoreactivation and dark repair of SR damage in airborne bacteria (Dimmick, 1960; Straat ef al., 1977) may contribute significantly to the increase in the airborne population of bacteria at Hanford. Additionally, two other factors may have contributed to the increase in the afternoon and evening viable bacterial concentration: stabilization of the ML depth with resultant decreased dilution effect; and increased wind (mechanical) turbulence, as opposed to

Bacterial flux morning heat (convective) turbulence causing an increase in the bacterial release rate. As the turbulence in the afternoon became more wind-driven, gusts that could produce a much higher short-term drag force (e.g. Shaw er al., 1975) on bacterial sources caused potential airborne bacteria adhering to plant and soil debris to be released to the atmosphere (Lighthart er al., 1994). The low numbers of bacteria found in the desert atmosphere is perhaps indicative of the harshness and relatively low production of the high desert environment. This is apparent when comparing the surviving fraction of the input flux bacteria from the high desert which was ca. 0.8 1% and a midwestern United States row crop field of beans, cu. 22.3%, and bare soil, cu. 18.7% (Lindemann et al., 1982). Thus the desert survival is approximately 20 times less than the midwestern row crop fields. This calculation suggests that further study of the effects of SR in conjunction with ambient temperature and RH is needed to predict bacterial survival in the atmosphere. In the first approximation, it appears that the daytime ML depth could have relatively little effect on the concentration of bacteria in the ML of the Hanford atmosphere during our observations. Assuming that the daytime 2000 m deep dynamic ML (e.g. Frisch et al., 1990) is homogeneous with respect to the input bacterial flux distribution, then maximum bacterial input flux of ca. 17,000 CFU me2 h- ’ indicates that the dilution effect on the ambient concentration would be ca. 8.5 CFU mm3 h-’ (= 17,000 CFU m-’ h- l/2000 m). This value is well below our observed values and within the noise level of our sampling system. In summary, the flux of bacteria from local plants and soil increases in the morning with convective turbulence to a relatively steady state. At the same time SR damage to the airborne cells increases until the damage rate equals the release rate (flux) at midday. This results in the population density minimum at that time. In the afternoon, the SR damage rate decreases until it is less than the release rate, the ML stabilizes, wind gusts increase, and the SR damage/repair ratio decreases. This appears as a dramatic increase in the bacterial concentration in the late afternoon. In the evening, the concentration of airborne bacteria increases in the atmosphere even though the release rate is nil. This may be because released bacteria may be trapped in the shallow stable nocturnal ML, larger particles that were transported to higher elevations may settle out, and finally those that are dark-repairable may be repaired. The temporal and spatial particle size distributions and bacterial taxa found during the Hanford observations will be the subject of future reports. We are beginning to understand the dynamics of natural populations of bacteria in the outdoor atmosphere. We now need to carry this further with additional measurements of the input flux of bacteria from other large-scale sources for extended periods, deter-

1273

mine the flux of bacteria out of the ML to large-scale sinks, and quantify the effect of such factors as SR, temperature, and RH that affect the survival of mixed populations of bacteria in the ambient extramural atmosphere. With this kind of information it will be possible to predict the atmospheric loading of airborne bacteria to avert or minimize microbial air pollution. Further, it is anticipated that methods similar to those used in this investigation will be used to evaluate the contribution of such agents as vegetation-applied microbial pesticides to microbial air pollution. AcColowledyemmts-We would like to thank Drs Brian Lamb of Washington State University, Pullman, WA; Monique LeClerc of The University of Quebec at Montreal, Canada; and Antony Delany and his staff at the National Center for Atmospheric Research, Boulder, CO, for allowing us to perform our research on their cooperative project to study micro-meteorological source footprints. We would also like to thank Dr L. Ganio of ManTech Environmental Technology Inc., at the U.S. EPA’s Environmental Research Laboratory. Corvallis. OR, for her superior statistical advice, and Dr A. S. Frisch of the Wave Propagation Laboratory, National Oceanographic and Atmospheric Administration, Boulder, CO, for his very helpful advice. For the excellent modifications made on our sampling tower, we would like to thank the TEAM, Inc. crew at the Environmental Research Laboratory, Corvallis, OR. Finally. we would like to thank Drs Lidia Watrud and Ann Fairbrother of EPA’s Environmental Research Laboratory. Corvallis. Oregon, for their support. The information in this document has been funded in part by the U.S. Army, Dugway Proving Ground, Dugway, UT and by the U.S. Environmental Protection Agency, Environmental Research Laboratory, Corvallis, OR. It has been subjected IO the Agency’s peer review and administrative review. and it has been approved for publication as an EPA document.

REFERENCES Anonymous (1991) Data results: revised bioaerosol monitoring program for the Washington suburban sanitary commission. Montgomery County Regional Composing Facility. Silver Spring, MD. Environmental Services Division, General Physics Corp. GP-R-341022. Businger J. A., Dabberot W. F., Delany A. C., Horst T. W., Martin C. L., Oncley S. P. and Semmer S. R. (1990) ASTER-the atmosphere-surface turbulent exchange research facility at NCAR. EOS 71, 693-702. Cox C. S. (1987) The Aerobioloyical Pathway of Microorganisms. p. 293. John Wiley & Sons, New York. Crowe J. H.. Carpenter F., Crowe C. M. and Anchordoguy T. J. (1990) Are freezing and dehydration similar stress factors? A comparison of modes 07 interaction of stabilizina solutes with biomolecules. Crrobiol. 21. 9-231. Dimmick R. L. (1960) Delayed recovery of airborne Serrafia marcescens after short-time exposure IO ultra-violet irradiation Science 4733, 251-252. Dimmick R. L. and Akers A. B. (1969) An Introduction to E.xperimenta/ Aerobioloyy, p. 494. Wiley Interscience, New York. Flexner J. L.. Lighthart B. and Croft B. A. (1986) The effects of microbial pesticides on non-target, beneficial arthropods. Ayric. Ecosyst. Encir. 16, 203-254. Freifelder D. M. (1987) Molecular Biology. Jones and Bartlett Publishers. Inc.. Boston.

1274

B. IXHTHART

Frisch A. S., Stankov B. B., Martner B. E. and Kaimal J. C. (1990) Doppler radar measurements of vertical velocity in the convective boundary layer. PrPprint volume of the Ninth Symposium 3 May. Roskilde.

on Turbulence and Diffusion. Denmark. pp. 82-85. American

30 April-

Meteorological Society, Boston. Fulton J. D. (1966a) Microorganisms of the upper atmosphere. IV. Microorganisms of a land air mass as it traverses an ocean. Appl. Microbial. 13, 241-244. Fulton J. D. (1966b) Microorganisms of the upper atmo sphere. V. Relationship between frontal activity and the micropopulation at altitude. Appl. Microbial. 14,245-250. Fulton J. D. and Mitchell R. B. (1966) Microorganisms of the upper atmosphere. II. Microorganisms in two types of air masses at 690 meters over a city. Appl. Microbial. 14, 232-236. Gregory P. H. (1973) Microbiology o/the Atmosphere, 2nd edn. p. 377. John Wiley & Sons, New York. Harm W. (1969) Biological determination of the germicidal activity of sunlight. Rad. Res. 40, 63-69. Huebert B. J. and Robert C. H. f1985) The drv deuosition of nitric acid to grass. J. geophyi. Res. W@lj, 2d85-2090. Huebert B. J.. Luke W. T.. Delany A. C. and Brost R. A. (1988) Measurements of concentrations and dry surface fluxes of atmospheric nitrates in the presence of ammonia. J. geophys. Res. 93(D6), 7127-7136. Israeli E., ShalTer B. T. and Lighthart B. (1993) Protection or freeze-dried Eschericllia co/i by trehalose upon exposure to environmental conditions. Cryobiol. 30, 519-523. Jagger J. (I 983) Physiological effects of near-ultraviolet radiation on bacteria. In Photochemical and Photobiological reviews, Vol. 7. pp. l-74. Plenum Press. New York. Kelly C. D. and Pady S. M. (1954) Microbiological studies of air masses over Montreal during 1950 and 1951. Can. J. Botany 32, 591-600. LeClerc M., Finn D. and Lamb B. (1992) Verification of the source footprint model. Presented at the Tenth Symposium on Turbulence and Diffusion, American Meterological Society, Portland, OR. Lighthart B. (1984) Microbial aerosols: estimated contribution of combine harvesting to an airshed. Appl. enuir. Microbial.

47, 430-432.

Lighthart B., Shafer B. T., Marthi B. and Ganio L. M. (1994) Artificial wind-gust liberation of microbial bioaerosols previously deposited on plants. Aerobiol. (in press). Lindemann J., Constantinidou H. A., Barchet W. R. and Upper C. D. (1982) Plants as sources of airborne bacteria, including ice nucleation-active bacteria. Appl. enuir. Microbial. 44, 1059-1063. Miller J. C. (1990) Field assessment of the effects of a microbial pest control agents on nontarget Lepidoptera. Am. Enfomol. Summer; l35- 139. Pady S. M. and Kramer C. L. (1967) Diurnal periodicity of airborne bacteria. Mycologia 59, 714-716. Pollard E. C. (1974) Cellular and molecular effects of solar ultraviolet radiation. Photochem. Phorobiol. 20, 301-308.

and B. T. SHAFFER Sharp D. G. (1940) The effects of ultraviolet light on bacteria suspended in air. J. Bocteriol. 39, 535-547. Shaw R. H.. Ward D. P. and Avlor D. E. llY75) Freauencv of occurrence of fast gusts of w&d inside a corncano’py. Abpl. Met. 18, 167-169. Straat P. A., Wolochow H.. Dimmick R. L. and Chatigny M. A. (1977) Evidence for incorporation of thymidine into deoxyribonucleic acid in airborne bacterial cells. Appl. envir.

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Stull R. B. eorology, Webb S. J. bacteria.

(1988) An Introducrion 10 Boundary Layer Metp. 666. Kluwer, Boston, MA. (1961) Factors aflectine. the viabilitv of air-borne ‘V. Tde inactivation anld reactivation of air-borne Serratia marcescens by ultraviolet and visible light. Can. J. Microbial. 26, 307-313. Webb S. J. and Lorenz J. R. (I 970) Oxygen dependence and repair of lethal effects of near ultraviolet and visible light. Photochem. Pholobiol. 12, 283-289. Wolf H. W.. Skaliy P., Hall L. B.. Harris M. M., Decker H. M., Buchanan L. M. and Dalgren C. M. (1964) Sampling microbiological aerosols. U.S. Dept. Health, Education and Welfare, Publ. Health Monograph No. 60, p. 53.

APPENDIX

The following are the least-squares best-fit equations used to represent the observations Hanford Nuclear Reservation, Richland, WA. tions of time-series (t) in 2400 h clock time: CFU=

concentration (in CFU me’) -242.7075+132.8554*~-16.8162*~L+0.8137*r3 -0.0128*1”; RZ = 0.48.

Bacrerialjux ki=Q,,,=

(in CFU m-‘h-‘) 763E+5-2.71E+5*r+3.41E+4*r2-l.80E

Bacteria/

+3*t3+33.7817*t4;

polynomial made at the All are func-

R’=0.72.

Solar radiation (in W m- *) SR =Q* =3435.30311516.646l*r

+226.4231*t2

- 12.6318

*t’ Sensible

+ 0.2342*r4;

R2 = 0.96.

heat f7u.x (in W m-l)

w’T’=Q,,=431.1192-262.0713*t+44.9645*12 -2.6356*~30.0495*r4;RZ=0.89. z/L (dimensionless)

z/L=2.6365-0.5295*r+0.0097*~2+0.0013tJ-4.026E5f4; R2 = 0.67. Temperature (in “C) T= -4.6869+ 5.7358*1-0.2990*? humidity (in %) RH=47.6076-4.7906*~+0.1510*r2;

+0.0051*t3.

Relative

RZ=0.59.

R2 =0.70.