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The Environmental Reporter
Volume 10 | Issue 1

I hope you're doing well and enjoying the new year. I also hope that you'll find the following article about winter aerosols by Dr. Harriet Burge both interesting and useful.

With best wishes,
Dave Gallup

Outdoor Spore Aerosols in Winter
By Dr. Harriet Burge, EMLab P&K Chief Aerobiologist and Director of Scientific Advisory Board

Outdoor aerosols, of both biological and chemical nature, nearly always affect those indoors. Throughout most of the year, outdoor fungal aerosols exceed those indoors by varying amounts, depending on many different factors. Important among these factors are the strengths of outdoor spore sources, release mechanisms that are active and removal factors.

In winter, some of these factors may be at their lowest, depending on seasonal and meteorological effects. Aerobiologists have traditionally used winter seasons to evaluate indoor aerosols, believing that the outdoor aerosol is least concentrated during winter. This is certainly true in areas where subfreezing temperatures and snow cover are consistent throughout the winter season.

Unfortunately, even a short thaw can mediate the release of intense fungal aerosols. For example, in England where snow and freezing temperatures may alternate with rain and above freezing temperatures, Penicillium/Aspergillus spores are present in outdoor air throughout the year (Millington & Corden 2005). Making a decision about whether or not to collect an outdoor control sample depends on understanding the factors that control outdoor aerosols for the region in which the sample is being collected. We offer here a brief summary of the factors influencing outdoor winter aerosols.

Overall climate patterns
Needless to say, outdoor winter aerosols are likely to be very different in (for example) Maine and Florida or Montana and California. Clearly, the only parts of the country where winter aerosols are likely to be low enough to be ignored are those where winter temperatures consistently stay below freezing for the winter and where snow cover is present most of that time. This discussion will be restricted to these areas.

Factors likely to affect winter aerosols
As mentioned above, source strength, inherent release, external release, and removal mechanisms are important factors. We also must include long distance transport.

Source strength
There are always sufficient fungal spores in outdoor environmental sources to produce significant aerosols, provided the sources are exposed to the air. The concentration of spores in the sources may, however, vary due to many factors including temperature regimes, light/dark patterns, maturation levels, and many others. Because plants tend not to grow as actively in the winter as in other seasons, we often ascribe this tendency to the fungi as well. Many fungi are dormant in winter, however others (including Stachybotrys), are cold-tolerant and compete well in near freezing temperatures. Many yeasts are active at cold temperatures, and in fact, are abundant in arctic ice (Butinar et al., 2011).

Many fungi, especially those that are abundant in cold climates, produce spores only during specified seasons. Septoria tritici Berk. & M.A. Curtis, blotch of winter wheat, is caused by Mycosphaerella graminicola (Fuckel) J. Schröt. which is the sexual (teleomorph) state of Septoria tritici. Epidemics of this disease begin in late autumn, with inoculation of new plants continuing throughout the early winter. Both ascospores (the Mycosphaerella state) and conidia (the Septoria state) of this fungus may be found in winter aerosols (Suffert et al., 2011).

Inherent periodicity
Periodicity in fungal spore production and inherent release mechanisms can lead to bursts of spore production during winter thaws. Some ascomycetes produce mature spores in the late fall. When this occurs, followed by a late winter thaw, these spores may be released in great abundance.

Splash dispersal
Fall maturing ascocarps release spores in response to fall rains. Subsequent aerosols are produced by rain splash. These rain splash events could presumably occur during winter rainfall as well (Inman et al., 1999). The so-called "phylloplane fungi" that occupy both living and dead plant material throughout the year may also be splash-dispersed during the winter, assuming any spores remain on the organic matter. A winter thaw could allow production of new spores that could also be splash-dispersed.

Mechanical agitation
Agricultural practices are well known to produce spore aerosols. Feeding cows during winter in alpine areas produces significant aerosols that could easily confound indoor samples, considering that the farmers then enter the indoor environment (Roussell et al., 2011). Activities at waste composting facilities could have the same effect during the winter.

Long distance transport
Although there is little, if any, phylloplane environment in Antarctica, fungal aerosols are commonly present. The most frequently encountered fungal genera include Penicillium, Aspergillus, Cladosporium, Alternaria, Aureobasidium, Botryotrichum, Botrytis, Geotrichum, Staphylotrichum, Paecilomyces and Rhizopus (Pearce et al., 2009). These fungi have traveled long distances through the air from their natural sources to the Antarctic. Other studies have documented Cladosporium spore aerosols that have traveled from England to Denmark, a distance of 650km (Carlile et al., 2001).

Maldonado-Ramirez et al. (2005) studied Fusarium spores over a range of 50m to 1km, simulating the planetary boundary layer, and evaluated the potential of long distance transport of plant disease. Long distance transport of desert dust has also been documented (Kellogg & Griffin 2006).

We have used our MoldRange data on outdoor spore concentrations to evaluate winter spore aerosols in Maine, a state where (except in coastal areas) snow cover and freezing temperatures are the rule rather than the exception during the period from December through February. The most abundant spore types during these months in Maine were basidiospores, ascospores, Cladosporium spp. and Penicillium/Aspergillus type spores. The table below provides a summary:

Spore type Median Maximum
Basidiospores 107 28089 72
Cladosporium 53 14613 58
Ascospores 107 4320 41
Pen/Asp 107 1680 76

*Percent of spores recovered from 287 samples

This graph below depicts spore concentrations from our database for winter samples in Maine. Only data from December-February are included to emphasize the range of aerosols that occur in the winter.

Spore Concentrations for Winter Samples in Maine

If spore levels are below detection limits outdoors, and such low levels are representative for the location and time of year, then one can assume that indoor aerosols on that day probably did not come in from outdoors. Note, however, that you cannot use the outdoor data as a mathematical control for indoors. You would be dividing by zero, which doesn't make sense.

If spore levels are above the detection limit, and are representative of the location and time of year, then you can use indoor/outdoor statistical methods. Extreme caution must be used, however, if the outdoor levels are low (less than about 200 spores/m3). These low outdoor levels may lead to indoor/outdoor ratios that are falsely high.

Since outdoor spore concentrations do appear to be well above zero during the winter months in a cold climate state like Maine, then it would be sensible to collect an outdoor sample for comparison, keeping in mind the location and time of year.

Practical decision-making
So if you live in an area where subfreezing temperatures and snow cover are consistent, AND you are reasonably sure that long distance transport doesn't affect your area, then you could omit outdoor sampling. Of course, then you cannot use the outdoor air as a control (i.e., indoor/outdoor ratios cannot be used). If conditions are, or recently have been different from these, I would suggest collecting the usual outdoor control sample. It is certainly better to be safe than sorry.

1. Butinar L, Strmole T, Gunde-Cimerman N. 2011. Relative incidence of ascomycetous yeasts in arctic coastal environments. Microbial Ecology 61:4):832-843.

2. Carlile MJ, Watkinson SC, Gooday GW. 2001. The Fungi. Academic Press, San Diego. Inman AJ, Fitt BDL, Todd AD, Evans RL. 1999. Ascospores as primary inoculum for epidemics of white leaf spot (Mycosphaerella capsellae) in winter oilseed rape in the UK. Plant Pathology 48(3):308-319.

3. Kellogg CA, Griffin DW. 2006. Aerobiology and the global transport of desert dust. Trends in Ecology & Evolution 21(11):638-644.

4. Maldonado-Ramirez SL, Schmale DG, Shields EJ, Bergstrom GC. 2005. The relative abundance of viable spores of Gibberella zeae in the planetary boundary layer suggests the role of long-distance transport in regional epidemics of Fusarium head blight. Agricultural and Forest Meteorology 132(1-2):20-27.

5. Millington WM, Corden JM. 2005. Long term trends in outdoor Aspergillus/Penicillium spore concentrations in Derby, UK from 1970 to 2003 and a comparative study in 1994 and 1996 with the indoor air of two local houses. Aerobiologia 21(2):105-113.

6. Pearce DA, Bridge PD, Hughes KA, Sattler B, Psenner R, Russell NJ. 2009. Microorganisms in the atmosphere over Antarctica. FEMS Microbiology Ecology 69(2):143-157.

7. Roussel S, Sudre B, Reboux G, Waser M, Buchele G, Vacheyrou M, Dalphin JC, Millon L, Braun-Fahriander C, von Mutius W, Piarroux E. 2011. Exposure to moulds and actinomycetes in Alpine farms: A nested environmental study of the PASTURE cohort. Environmental Research 111(6):744-750.

8. Suffert F, Sache I, Lannou C. 2011. Early stages of Septoria tritici blotch epidemics of winter wheat: build-up, overseasoning, and release of primary inoculum. Plant Pathology 60:166-177.

The data and other information contained in this newsletter are provided for informational purposes only and should not be relied upon for any other purpose. EMLab P&K hereby disclaims any liability for any and all direct, indirect, punitive, incidental, special or consequential damages arising out of the use or interpretation of the data or other information contained in, or any actions taken or omitted in reliance upon, this newsletter. Images included in this newsletter are property of EMLab P&K, unless otherwise specified.

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