ArticlePDF Available

Fungal spores are transported long distances in smoke from biomass fires

February 2004
Atmospheric Environment 38(5):651-655

DOI:10.1016/j.atmosenv.2003.10.043

Authors:

Sarah A Mims

Forrest M. Mims III

Geronimo Creek Observatory

Viable fungal spores are present in smoke from distant biomass fires. This finding has potentially important implications for prescribed burning, agricultural management and public health. While attempting to find fungal spores in dust blown from China to Texas, one of us (S.A.M.) discovered that smoke from Yucatan contains viable bacteria and fungal spores, including the genera Alternaria, Cladosporium, Fusariella and Curvularia. There was a high correlation (r2=0.78) of spores and coarse carbon particles collected on microscope slides during 13 days of the 2002 smoke season. To eliminate possible contamination by local spores, an air sampler was flown from a kite at a Texas Gulf Coast beach during and after the 2003 smoke season on days when the NOAA back trajectory showed air arriving from Yucatan. Fifty-two spores and 19 coarse black carbon particles (>2.5 μm) were collected during a 30-min kite flight on the smoke day and 12 spores and four carbons on the day without smoke. We have found spores in smoke from an Arizona forest fire and in Asian smoke at Mauna Loa Observatory, Hawaii. We have tested these findings by burning dried grass, leaves, twigs and flood detritus. The smoke from all test fires contained many spores.

Xy scattergraph ( r 2 1⁄4 0 : 78) of fungal spores and coarse

…

On days when the NOAA back trajectory (a,b) indicated air arrived at North Padre Island, Texas, from Yucatan 48 h earlier (4 May and 5 August 2003), an air sampler was flown from a kite at a Gulf Coast beach when smoke from Yucatan was present (c) and not present (d). During 30-min flights, the sampler collected 52 spores and 19 coarse carbons on the smoke day (e), and only 12 spores and four carbons on the nonsmoke day (f).

…

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Atmospheric Environment 38 (2004) 651–655

Fungal spores are transported long distances in smoke from

biomass ﬁres

Sarah A. Mims, Forrest M. Mims III*

Geronimo Creek Observatory, 433 Twin Oak Road, Seguin, TX 78155, USA

Received 1 October 2003; received in revised form 20 October 2003; accepted 22 October 2003

Abstract

Viable fungal spores are present in smoke from distant biomass ﬁres. This ﬁnding has potentially important

implications for prescribed burning, agricultural management and public health. While attempting to ﬁnd fungal spores

in dust blown from China to Texas, one of us (S.A.M.) discovered that smoke from Yucatan contains viable bacteria

and fungal spores, including the genera Alternaria, Cladosporium, Fusariella and Curvularia. There was a high

correlation (r2¼0:78) of spores and coarse carbon particles collected on microscope slides during 13 days of the 2002

smoke season. To eliminate possible contamination by local spores, an air sampler was ﬂown from a kite at a Texas

Gulf Coast beach during and after the 2003 smoke season on days when the NOAA back trajectory showed air arriving

from Yucatan. Fifty-two spores and 19 coarse black carbon particles (>2.5 mm) were collected during a 30-min kite

ﬂight on the smoke day and 12 spores and four carbons on the day without smoke. We have found spores in smoke

from an Arizona forest ﬁre and in Asian smoke at Mauna Loa Observatory, Hawaii. We have tested these ﬁndings by

burning dried grass, leaves, twigs and ﬂood detritus. The smoke from all test ﬁres contained many spores.

Keywords: Prescribed ﬁres; Agricultural ﬁres; Public health; Carbon; Dust

1. Introduction

We have found that convection caused by biomass

ﬁres can launch fungal spores and bacteria skyward,

where they may travel thousands of kilometers. While

the long-distance transport of fungal spores on currents

of air is well established (Meier and Lindbergh, 1935;

Brown and Hovmoller, 2002), we are unaware of a prior

publication that describes ﬁre-induced convection as a

mechanism for initiating such long-distance transport.

Karnal bunt, a smut infection of wheat caused by

Tilletia indica, can spread by convection to surrounding

ﬁelds when diseased wheat is burned (Roux and

O’Brien, 2001). This disease has spread around the

world from its origin in India, and the ﬁndings reported

here suggest that ﬁre-induced convection might spread

pathogenic spores much greater distances than sur-

rounding ﬁelds.

Sugarcane rust caused by the fungus Puccinia

melanocephala, appeared in the Dominican Republic in

July 1978. Purdy et al. (1985) suggest this outbreak

followed transoceanic transport of spores from West

Africa. Because sugarcane is burned at harvest, we

suggest that convection caused by ﬁre could have

launched spores into the air stream that delivered

inoculum to the Caribbean. Burning of diseased plants

is so widespread, and often mandated, that there are

many similar scenarios for the launching of pathogenic

microbes by ﬁre-induced convection.

There is an abundant literature on long-distance

transport of fungi that are pathogenic to plants and

that cause allergic reactions when inhaled by people

(Kendrick, 2000;Grifﬁn et al., 2001;Brown and

Hovmoller, 2002). Microbes are unique among particulate

ARTICLE IN PRESS

*Corresponding author. Tel.: +1-830-372-0548; fax: +1-

830-372-2284.

E-mail address: forrest.mims@ieee.org (F.M. Mims III).

doi:10.1016/j.atmosenv.2003.10.043

matter, for, unlike nonviable particles, microbes can

rapidly multiply. Thus, the transport of a small number

of pathogenic spores can result in the eventual infection

of entire ﬁelds. This phenomenon is well known and can

sometimes be forecast. For example, the North Amer-

ican Plant Disease Forecast Center at North Carolina

State University publishes on the Internet forward

trajectories of Pseudoperonospora cubensis, which causes

Downy mildew in squash, cucumbers, pumpkins, and

muskmelons, and Peronospora tabacina Adam, which

infects tobacco (Main et al., 2001). Similar forecasts

might be relevant to smoke events.

2. Fungal spores and Central American smoke

Fungal spores and bacteria are associated with dust

that originates in North Africa and reaches the

Caribbean. Grifﬁn et al. (2001) discuss bacteria and

spores associated with Sahara dust transported across

the Atlantic. Shinn et al. (2000) describes how the soil

fungus Aspergillus in Sahara dust infects Caribbean

coral reefs. During a study in April 2002 to determine if

viable microbes are transported with dust transported

from Asia to Texas, one of us (S.A.M.) serendipitously

discovered many viable fungal spores and bacteria

associated with smoke arriving at Geronimo Creek

Observatory in South-Central Texas (29.6N, 97.9W)

from large ﬁres in Yucatan, Mexico.

2.1. Central American smoke at Central Texas, 2002

During the April 2002 smoke event, the Navy Aerosol

Analysis and Prediction System (NAAPS) aerosol

forecast model (US Naval Research Observatory,

www.nrlmry.navy.mil/aerosol/) showed that the smoke

originating in Yucatan traveled some 1450 km and

reached Geronimo Creek Observatory in 2–3 days.

The smoke reduced visibility, increased the optical depth

measured by Sun photometers, created a pronounced

solar aureole, and caused sharp increases in the number

of 0.5 mm particles.

On 13 days during this event, a microscope slide was

placed on a 4-m meteorological tower in an open ﬁeld to

collect coarse carbon particles (diameter >2.5 mm) and

spores. At local noon, two nutrient media ﬁlms (3 M

Petriﬁlms (TM)), one formulated for bacteria (Petriﬁlm

Aerobic) and one for fungi (Petriﬁlm Yeast and Mold),

were hydrated with distilled water, exposed for 15 min

on the tower, and incubated 3 days at ambient

temperature.

Many colonies of fungi and bacteria grew on the ﬁlms

exposed during the smoke episode. The microscope

slides permitted the numerical relationship of the spores

and coarse carbon particles in the smoke to be

quantiﬁed. Four scans across the width of each slide

were made, and all spores and coarse carbon particles

were counted. Fungal spores included representatives

from 22 genera, including Alternaria, Cladosporium,

Fusariella, Nigrospora, and Curvularia. As shown in

Fig. 1, the correlation of all coarse carbon particles and

spores deposited on slides during the smoke episode was

very high (r2¼0:78). However, the correlation of some

genera with carbon particles was very low (e.g., r2¼

0:00 and 0.05). These were likely local in origin.

2.2. Central American smoke at Texas Gulf Coast, 2003

Smoke from Yucatan again reached Texas during

May 2003. A passive air sampler designed by S.A.M.

was ﬂown from a kite over a beach at North Padre

Island, Texas (27.4N, 97.3W), on days when smoke from

Yucatan was present and not present to eliminate

interference from spores originating in Texas. Fig. 2

summarizes the kite experiments.

On 3 May 2003 (Fig. 2a, c and d), NOAA back

trajectories showed that air at the Texas Gulf Coast had

passed over Yucatan 48 h earlier. Terra MODIS and

SeaWiFS imagery showed that smoke from ﬁres in

Yucatan covered the Western Gulf of Mexico. During

the kite ﬂight, a nearby monitoring station (CAMS 341)

operated by the Texas Commission on Environmental

Quality measured 16.1 mg/m

of PM 2.5 particles in air

arriving from over open water at a mean direction of

134. A 30-min ﬂight captured 52 fungal spores and 19

coarse carbon particles (Fig. 2e).

On 5 August 2003, the NOAA back trajectory again

showed air coming from Yucatan. Terra MODIS

imagery showed no major ﬁres in Yucatan and the

study site. During the kite ﬂight, CAMS 341 measured

5.5 mg/m

of PM 2.5 particles in wind arriving from over

open water at a mean direction of 161. A 30-min ﬂight

captured 12 fungal spores and four coarse carbon

particles (Fig. 2f).

ARTICLE IN PRESS

Fig. 1. Xy scattergraph (r2¼0:78) of fungal spores and coarse

carbon particles deposited by sedimentation on exposed

microscope slides at Geronimo Creek Observatory in South

Central Texas on all 13 days samples were collected from 25

April–10 May 2002 during a major Central American smoke

event.

S.A. Mims, F.M. Mims III / Atmospheric Environment 38 (2004) 651–655652

Spores collected by the kite sampler include many of

those collected during the 2002 Yucatan smoke event,

including the genera Alternaria, Cladosporium,Fusar-

iella and Curvularia. The kite study provides compelling

evidence that spores were present in smoke from

Yucatan arriving at the Texas Gulf Coast.

3. Fungal spores in other smoke events

We collected fungal spores in smoke from a forest ﬁre

in Arizona (18 June 2003) and in smoke from Canada

and Louisiana at College Station, Texas (10 August

2003). We collected Alternaria and other spores and

carbon particles at Mauna Loa Observatory (MLO),

Hawaii (elevation 3400 m), during a rare Asian smoke

event (6 July 2003). The smoke formed distinct layers

and was associated with high concentrations of ozone

(>70 ppb), which were highly correlated (r2¼0:98)

with the 5 mm particle count.

4. Experimental validation of fungal spores in smoke

A simple experiment was designed to determine if

fungal spores and bacteria are present in smoke from

burning grass. Four Petriﬁlms (two bacteria and two

mold) were clipped to a horizontal pole and exposed to

smoke from burning grass for 5 min. A second set of

four Petriﬁlms was exposed to background air for 5 min.

ARTICLE IN PRESS

Fig. 2. On days when the NOAA back trajectory (a,b) indicated air arrived at North Padre Island, Texas, from Yucatan 48 h earlier

(4 May and 5 August 2003), an air sampler was ﬂown from a kite at a Gulf Coast beach when smoke from Yucatan was present (c) and

not present (d). During 30-min ﬂights, the sampler collected 52 spores and 19 coarse carbons on the smoke day (e), and only 12 spores

and four carbons on the nonsmoke day (f).

S.A. Mims, F.M. Mims III / Atmospheric Environment 38 (2004) 651–655 653

After 3 days of incubation at ambient temperature, the

ﬁlms exposed to smoke had a total of >115 mold and

>90 bacteria colony forming units (CFUs). Those

exposed to background air had only 10 mold and eight

bacterial CFUs.

Various kinds of biomass were placed on a steel plate

in an open ﬁeld and burned. Smoke from each ﬁre was

sampled for 1 min using three Petriﬁlms (mold only).

The temperature of the ﬁlms, which was monitored with

noncontact IR thermometry, ranged from 34Cto49

C.

Between ﬁres, the background air was sampled for 1 min

using three Petriﬁlms. A wood walkway prevented

contamination by local spores. After 3 days of incuba-

tion at ambient temperature, nutrient ﬁlms exposed to

smoke from all the biomass samples exhibited signiﬁ-

cantly more CFUs than those exposed to ambient air

between burns. The ratios of total CFUs in smoke to

CFUs in background air were 9:3 (dry grass), 19:0 (dry

leaves), 48:4 (twigs) and 87:5 (ﬂood detritus).

Our observations and photographs of test ﬁres under

a plant canopy suggest that agitation of leaves caused by

turbulent convection (Pisaric, 2002) may dislodge

spores, which are then carried upward with the warm

plume. Nearer the ground, turbulent air rushing in to

feed the ﬂames may also carry spores into the smoke

plume.

5. Conclusions

The common assumption that plant pathogens are

killed by burning is contradicted by the spread of Karnal

bunt to surrounding ﬁelds when wheat infected with T.

indica is burned (Roux and O’Brien, 2001). Our ﬁndings

of many fungal spores in smoke from all test ﬁres, and

from large ﬁres in Yucatan more than 1500 km distant,

suggest that plant pathogens might be spread consider-

ably farther than surrounding ﬁelds. Some fungal spores

we have found in smoke (e.g., Alternaria) cause allergic

reactions and trigger asthma attack (Kendrick, 2000).

Heretofore, such reactions have been attributed solely to

smoke inhalation, and we propose that fungal spores

may also play a role. We propose to test this hypothesis

by comparing emergency department visits for asthma

and allergy-related respiratory incidents with spore

counts by the Aeroallergen Monitoring Network of the

American Academy of Allergy, Asthma and Immunol-

ogy (Anon, 2001), which reveal examples of high mold

counts during smoke events. This study will also

examine incidence of asthma attack in the weeks after

major smoke events, for the progeny of spores

transported with smoke might be an even greater

problem.

Prescribed burns of diseased crops, brush, timber,

slash and rubbish may disperse large numbers of

pathogenic fungi. Major ﬁres, which can produce smoke

plumes 3 km or more high, could be much more effective

in launching spores into the troposphere than surface

wind storms. Small burns of diseased plants and cooking

and heating with diseased ﬁrewood might disperse

pathogenic spores on a smaller scale.

A beneﬁcial role for spores carried skyward with

forest ﬁre smoke could be reinoculation of ﬁre-sterilized

soil with mycorrhizal fungi and the dispersal of

such symbiotic fungi to new locations. We plan to

test this hypothesis. We also plan to study the

variety and number of spores and bacteria in smoke

from various kinds of ﬁres. The abundance of spores

relative to coarse carbon particles, 3:1 for Yucatan

smoke in Texas and 1:1 for Asian smoke at MLO,

could have a slight inﬂuence on radiative transfer

models, for spores are regularly shaped and often

translucent, while coarse carbon is opaque, black and

irregularly shaped.

Acknowledgements

Tom Gill informed us that Central American smoke

was present when fungal spores were ﬁrst found in

smoke. Mark Hartwig suggested the design hypothesis

that dispersal in smoke of mycorrhizal fungal spores

might be beneﬁcial. John Barnes facilitated sampling at

Mauna Loa Observatory. Gabriel Solis and Ryan

Peschel assisted with test ﬁres. Gerald Holmes informed

us about the spread of Karnal bunt by burning. We

thank those responsible for NOAA back trajectories,

GSFC MODIS imagery and the NRL NAAPS model.

We also thank Eugene Shinn for helpful discussions and

the editor and two anonymous reviewers for suggestions

that greatly improved the manuscript.

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Blue mold of tobacco, also known as 'mildiou du tabac' in Europe(16,18,21,31,33), caused by Peronospora tabacina Adam, is a classical compound-interest plant disease that develops local as well as macroscale epidemics (4,11) (Fig. 1). The fungus is highly weather-sensitive. During periods of cool, wet, and overcast weather the disease can develop in greenhouses and/or fields and spread rapidly because of the polycyclic nature of the fungal pathogen (2,16,17). The rate of continental spread is largely determined by the potential for high levels of initial source inoculum (Fig. 2), short latent period, effective wind dispersal of spores and approximately 500,000 acres of susceptible tobacco fields across the eastern half of the United States and Canada. When the weather becomes clear, dry, and hot, the epidemic usually slows considerably or stops completely. Commercial tobacco is a seasonal crop in the temperate, humid farming zones of the Southeastern and Eastern United States, Canada, and tropical countries bordering the Caribbean basin. Following a crop-free period (winter) each year in the U.S., tobacco is exposed to asexual, windborne sporanagiospores (Fig. 3) that are believed to originate from inoculum sources of commercial winter tobacco in the tropical production zones south of the 30th parallel of latitude (22,26) and wild Nicotiana species (17,28) in the southwestern United States. It is unlikely that the fungus overwinters in the more temperate zones north of the 30th latitude because oospores have not been found in the U.S. Inoculum is therefore believed to be introduced into the U.S. anew each year (11) (Fig. 4). Further research is needed to clearly elucidate the possible role of oospores in blue mold epidemics. Research on the epidemiology and biometeorology of tobacco blue mold at N.C. State University began in 1981 following severe continent-wide epidemics in 1979 and 1980 (6,9,19). Moss and Main (27) demonstrated that a new high-temperature biotype of P. tabacina caused an early spring plant bed disease to develop into a serious summer production problem. The blue mold forecasting system was made available to all growers and the industry in 1995 (24). In 1998, a similar forecasting system for downy mildew of cucurbits was developed. Macroscale epidemics of blue mold have occurred each year since 1979 (5). The impact of these two pathogens each year largely depends upon the time of inoculum arrival and frequency of favorable weather conditions on the North American continent.

African dust and the demise of Caribbean Coral Reefs

Article

Full-text available

Oct 2000
GEOPHYS RES LETT

The vitality of Caribbean coral reefs has undergone a continual state of decline since the late 1970s, a period of time coincidental with large increases in transatlantic dust transport. It is proposed that the hundreds of millions of tons/year of soil dust that have been crossing the Atlantic during the last 25 years could be a significant contributor to coral reef decline and may be affecting other ecosystems. Benchmark events, such as near synchronous Caribbean-wide mortalities of acroporid corals and the urchin Diadema in 1983, and coral bleaching beginning in 1987, correlate with the years of maximum dust flux into the Caribbean. Besides crustal elements, in particular Fe, Si, and aluminosilicate clays, the dust can serve as a substrate for numerous species of viable spores, especially the soil fungus Aspergillus. Aspergillus sydowii, the cause of an ongoing Caribbean-wide seafan disease, has been cultured from Caribbean air samples and used to inoculate sea fans.

African desert dust in the Caribbean atmosphere: Microbiology and public health

Article

Full-text available

Sep 2001

Air samples collected on St. John in the U.S.Virgin Islands were screened for the presenceof viable bacteria and fungi to determine ifthe number of cultivatable microbes in theatmosphere differed between ``clear atmosphericconditions'' and ``African dust-events.'' Resultsindicate that during ``African dust-events,'' thenumbers of cultivatable airborne microorganismscan be 2 to 3 times that found during ``clearatmospheric conditions.'' Direct microbialcounts of air samples using an epifluorescentmicroscopy assay demonstrated that during an``African dust-event,'' bacteria-like andvirus-like particle counts were approximatelyone log greater than during ``clear atmosphericconditions.'' Bacteria-like particles exhibitingautofluoresence, a trait of phototrophs, wereonly detected during an ``African dust-event.''

Collecting micro-organisms from the Arctic atmosphere

Article

Purdy LH, Krupa SV, Dean JL.. Introduction of sugarcane rust into the Americas and its spread to Florida. Plant Dis 69: 689-693

Article

Jan 1985
PLANT DIS

L. H. Purdy

Long-distance transport of terrestrial plant material by convection resulting from forest fires

Article

Jan 2002

Michael F J Pisaric

Paleoecologists widely accept macroscopic plant remains preserved in lake sediment as good indicators of the vegetation communities growing within and adjacent to the margin of a lake or mire. However, the study of ash fallout from a small to moderate size forest fire in a low elevation Pseudotsuga menziesii/Pinus contorta/Abies lasiocarpa stand near Bozeman, Montana suggests that certain macroscopic plant remains can be transported long distances through the atmosphere. Conifer needles, pollen cones, cone scales, bracts and wood fragments were transported via the atmosphere and subsequently deposited at least 20 km from the forest fire. The majority of the plant remains that were identified were A. lasiocarpa needles. Pseudotsuga menziesii and P. contorta needles were also identified, but both were less abundant than A. lasiocarpa. The plant material that was recovered exhibited varying degrees of charring suggesting that it may be difficult to distinguish plant material that has been transported long-distances by forest fires from that which has been derived locally. Severe convection and vortices associated with intense forest fires are believed to be the primary mechanisms responsible for transporting plant material via the atmosphere.

Aerial Dispersal of Pathogens on the Global and Continental Scales and Its Impact on Plant Disease

Article

Aug 2002
SCIENCE

Some of the most striking and extreme consequences of rapid, long-distance aerial dispersal involve pathogens of crop plants. Long-distance dispersal of fungal spores by the wind can spread plant diseases across and even between continents and reestablish diseases in areas where host plants are seasonally absent. For such epidemics to occur, hosts that are susceptible to the same pathogen genotypes must be grown over wide areas, as is the case with many modern crops. The strongly stochastic nature of long-distance dispersal causes founder effects in pathogen populations, such that the genotypes that cause epidemics in new territories or on cultivars with previously effective resistance genes may be atypical. Similar but less extreme population dynamics may arise from long-distance aerial dispersal of other organisms, including plants, viruses, and fungal pathogens of humans.

Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease African desert dust in the Caribbean atmosphere: microbiology and public health The Fifth Kingdom. Mycologue Publica-tions

537-541

J K M Brown
M S Hovmoller
D W Griffin
V H Garrison
J R Herman
E A Shinn

Brown, J.K.M., Hovmoller, M.S., 2002. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297, 537–541. Griffin, D.W., Garrison, V.H., Herman, J.R., Shinn, E.A., 2001. African desert dust in the Caribbean atmosphere: microbiology and public health. Aerobiologia 17, 203–213. Kendrick, B., 2000. The Fifth Kingdom. Mycologue Publica-tions, Sydney, BC, Canada, pp. 126–141 (http://www. mycolog.com/). Main, C.E., Keever, T., Holmes, G.J., Davis, J.M., 2001

2000 AAAAI Pollen and Spore Report