Introduction
Most precipitation in the midlatitude and polar regions is linked to ice
formation in clouds (Field and Heymsfield, 2015). Biological particles
catalyse the freezing of supercooled cloud droplets at temperatures between
-1 and -15 ∘C, whereas other particles (e.g. mineral dust, soot)
are active at colder temperatures (Després et al., 2012; Murray et al.,
2012). The ice particles formed grow to snowflakes through vapour deposition
and, more rapidly, through riming and aggregation. A few initial ice
particles (< 10 m-3) catalysed at -8 ∘C near the cloud
top can rapidly glaciate a shallow supercooled cumulus (Mason, 1996; Crawford
et al., 2012). This is possible through explosive ice multiplication by
riming and splintering graupel pellets between -3 and -8 ∘C
(Hallett and Mossop, 1974). Therefore, ice-nucleating particles (INPs) active at
-8 ∘C or at warmer temperatures (from here on collectively
denominated as INP-8) could strongly influence precipitation
development, despite their usually small number concentration in the
atmosphere, for example compared to mineral dust or soot particles. The few
atmospheric data on INP-8 suggest that vegetated lands are stronger
sources than deserts (Conen et al., 2015), and that rainfall triggers the
aerosolisation of such INPs from forest (Hara et al., 2016). Aerosolisation is
probably due to the mechanical impact of raindrops on surfaces hosting
organisms that, as a whole or in parts, can serve as INPs. Increased
concentration during and after rainfall has also been demonstrated for INPs
active at colder temperatures (-15 ∘C) by Bigg and Miles (1964,
examined in more detail in Bigg et al., 2015) at 24 sites in Australia, and
by Huffman et al. (2013), Tobo et al. (2013) and Prenni et al. (2013) at a
site in Colorado, USA. Investigations at the latter site were accompanied by
detailed characterisation of aerosolised particles regarding their size
distribution, fluorescence, morphology and biological origin. Huffman et
al. (2013) suggested that “follow-up studies in other environments shall
elucidate whether the observed rain-related bioaerosol increase is a common
feature of terrestrial ecosystems or specific for the investigated semi-arid
environment”. Thus, we took this suggestion as a starting point to
investigate rainfall effects in the coastal climate of southern Norway.
Material and methods
Unlike previous studies, we continuously sampled aerosol particles over the
course of 15 months, from October 2013 to December 2014, on a filter replaced
once a week. The low time resolution of 1 week provided a large sampled
volume, which enabled the reliable detection of INP-8 in all samples.
Site description
The Birkenes Observatory (58∘23′ N, 8∘15′ E,
219 m a.s.l.) is situated approximately 20 km from the Skagerrak coast in
southern Norway (Fig. 1) and is located on a minor hilltop in an undulating
terrain, which allows for efficient ventilation and air mass mixing.
Kristiansand (61 000 inhabitants, 2016) is the nearest city, located 25 km
south/south-west of the station. The observatory is located in the
Boreonemoral zone with mixed coniferous and deciduous trees, accounting for
65 % of the land use near the site. Meadows and low-intensity agricultural
areas account for 10 % each, whereas 15 % are freshwater lakes. Birch is
the most common deciduous tree in the area around the observatory, for which
budding starts in late April and the shedding of leaves is over by mid-October.
Location of Birkenes Observatory (a) and a view of the
observatory (b).
By its proximity to the coast and low altitude, the Birkenes Observatory
experiences a coastal climate, with relatively mild winters (Tmean
Jan–Feb 2014 = -0.3 ∘C) and moderately warm summers
(Tmean Jun–Aug 2014 = 15.6 ∘C). The annual amount of
precipitation around Birkenes was 2077 mm in 2014, about 1.5 times the
normal (1961–1990) amount. Of this, 12 % precipitated as snow. The mean
temperature in 2014 exceeded the norm by 2–3 ∘C (MET, 2015). The
prevailing wind direction is from the west and the south-west, occasionally
with quite high wind speeds. Hence, the observatory is situated downwind of
major emission regions in continental Europe.
Aerosol sampling
Ambient aerosol filter samples were collected as part of the Norwegian
national monitoring programme (Aas et al., 2015), using two
Kleinfiltergerät low-volume samplers with a PM10 and a PM2.5
inlet to collect aerosols on prefired (850 ∘C; 3 h) single-quartz
fibre filters (Whatman QM-A; 47 mm in diameter). Both samplers operated at a
flow rate of 38 L min-1, corresponding to a filter face velocity of
47.3 cm s-1. Filters were conditioned at 20 ± 1 ∘C and
at 50 ± 5 % RH (relative humidity) for 48 h before and after
exposure. Filters were kept in petri slides for transportation and storage.
Post conditioning, filters were stored at 4 ∘C for approximately 1
month for subsequent analysis of OC / EC, then at -18 ∘C prior
to analysis of arabitol and mannitol.
Analysis of ice-nucleating particles
Number concentrations of INP-8 on PM10 and PM2.5 filter
samples were determined with 108 punches (1.0 mm diameter) from each filter.
Each punch was immersed in Milli-Q water (0.1 mL) in a tube (1.5 mL,
Eppendorf Safe-Lock), cooled from -4 to -12 ∘C
(0.3 ∘C min-1) in a cold bath (Lauda, model RC6). The number
of frozen tubes were counted every 1 ∘C temperature step to
calculate the number concentration of INPs in sampled air (Conen et al.,
2012). The punches from 10 filters in each size fraction were tested a second
time after they had been immersed for 10 min in a water bath at
90 ∘C. We also tested 24 field blanks the same way. Only one had a
small positive signal (0.08 INP-8 m-3) and 23 were negative at
-8 ∘C, thus we did not do a blank correction. As we have analysed
punches of each filter in two lots of 54, we can estimate the uncertainty of
our procedure. The mean deviation of INP-8 derived from single lots of
54 punches, from that of both lots taken together (108 punches), was 22, 19,
13 and 12 % for INP-8 < 1, 1 to 2, 2 to 4, and > 4 m-3,
respectively.
Analysis of arabitol and mannitol
Arabitol and mannitol have previously been identified as amenable tracers of
fungal spores (Bauer et al., 2008). Concentrations of arabitol and mannitol
in PM10 filter samples were determined using Waters Acquity
ultra-performance liquid chromatography (UPLC) in combination with Waters
Premier XE high-resolution time-of-flight mass spectrometry (HR-TOF-MS)
operated in the negative electrospray ionisation (ESI) mode: resolution
> 10 000 FWHM (full width at half maximum). The analytical methodology is
based on that described by Dye and Yttri (2005) for monosaccharide
anhydrides, deviating from the original one only by choice of the column
(2.1 × 150 mm HSS T3, 1.8 µm, Waters Inc.). Arabitol and
mannitol were identified on the basis of retention time and mass spectra of
authentic standards (ICN Biomedicals). Response factors for arabitol and
mannitol were calculated from external standards. Isotope-labelled standards
of levoglucosan (13C-levoglucosan, 98 %, Cambridge Isotopic
Laboratories) were used as the internal recovery standard.
FLEXPART
FLEXPART is a Lagrangian particle dispersion model (Stohl et al., 1998, 2005)
and is used to investigate the origin of air masses and their potential for
emission uptake. The model is driven by 1×1∘ operational
meteorological data from the European Centre for Medium Range Weather
Forecast (ECMWF) with 3 h temporal resolution and 137 vertical levels.
The model calculates the trajectories of tracer particles using the
interpolated mean winds plus random motions representing turbulence and moist
convection. The particles are subject to dry and wet deposition, the latter
of which is described in detail in Grythe et al. (2017).
For this study, FLEXPART was run for 20 days backward in time with a black carbon
tracer, which experiences wet and dry deposition. Black carbon was used as a
proxy for INPs, as both are susceptible to dry and wet scavenging. For the
exact time interval in which each filter sample was collected, 400 000 particles were
released. The FLEXPART output represents potential emission sensitivity in units of
seconds. It quantifies the impact of potential emissions on the aerosol
concentration at the measurement site. If multiplied with known emission
fluxes, the aerosol concentration at the receptor is obtained. Since
emissions of INPs are not known, we use arbitrary constant emission densities
for the different land use types, based on the International Geosphere-Biosphere
Programme (IGBP) data (Belward, 1999) at 1×1∘
resolution. The land use categories used are urban, agriculture, range land,
deciduous forest, mixed forest, coniferous forest, water, desert, wetland,
agriculture/range land, rocky areas, snow and rainforest. Our procedure thus
quantifies the relative impact that INP emissions in these land use types
would have on the INP concentration in a measurement sample.
Results and discussion
Time series of INP-8 and precipitation
Our observations revealed a general seasonal pattern. Values of INP-8 in
PM10 were mostly < 2 m-3 during spring and summer, and
> 4 m-3 over the course of several weeks during autumn. Values
decreased with snowfall in winter and were on average 1.2 m-3 as long
as the ground was covered by snow (Fig. 2). Elevated INP-8 levels of
short duration in spring and summer were associated with rainfall exceeding
20 mm per week. Similar rates of snowfall (January 2013) were not
accompanied by additional INP-8. Deposition velocity of snow is in the
order of 1 m s-1 (Garrett et al., 2012), while that of even a small raindrop
(1 mm diameter) is already four times as large (Gunn and Kinzer, 1949).
Hence, for the same mass, the kinetic energy of rain (proportional to the
velocity squared) is at least an order of magnitude larger compared to
precipitation in the form of snow, and so the energy is available for dispersion
and aerosolisation of particles.
Time course of INP-8 in the PM10 (black) and PM2.5
(green) particle size fractions. Peaks in INP-8 largely mirror peaks in
precipitation (blue is inverse scale to mirror precipitation values on the
horizontal axis). Snow (open circles) or small amounts of rain are
accompanied by very small numbers of INP-8 in the same week. Significant
amounts of snow on the ground (grey bars) seem to attenuate the increase in
INP-8 with intense rainfall. Total amount of precipitation in 2014 was
2077 mm (entire period shown: 2640 mm). Precipitation and snow cover data
are the averages of three stations operated by the Norwegian Meteorological
Institute in the municipality of Birkenes.
Hara et al. (2016) saw enhanced concentrations of INP-7 during
rainfall, but not during snowfall at Kanazawa, a coastal city in Japan.
Huffman et al. (2013) suggested that rainfall may trigger the release of INPs
from vegetation through its mechanical impact. Such impact happens on
leaves, but also on other surfaces, such as twigs, stems, soil and on leaf
litter covering the forest floor. If leaves on trees were the only relevant
source of INPs, we should have seen a marked decrease in atmospheric
concentrations once leaves were shed by mid-October. No change of this kind
was discernible in the autumn of 2013 or 2014. Numbers of INPs on shed leaves
increase substantially upon decay (Vali et al., 1976). At first sight, it
seems unlikely that INPs produced on the forest floor are transported above
the canopy. However, once trees are defoliated, raindrops hit the ground
with less interception by canopies, and turbulent momentum penetrates more
easily into the subcanopy layer (Staebler and Fitzjarrald, 2005). Continued
occurrence of large numbers of airborne INP-8 during the defoliated
period suggests that the reduced likelihood of aerosolisation from the
forest floor is largely compensated by the increased source strength of INPs
due to the decay of the shed leaves. Throughout the year, the increase in
INP-8 with weekly rainfall occurs despite the fact that scavenging of
such particles is also enhanced by rain.
An increase or decrease in the amount of rainfall from one week to the next
was followed in 76 % of all cases by a change in INP-8 in the same
direction (2013 and 2014, excluding weeks with snowfall; n = 58).
However, the change in INP-8 was not always proportional to the change
in rainfall. In particular, large amounts of rainfall during February 2014
had a relatively small effect. Snowfall in January had left the ground
covered with 1 m of snow, which diminished during February and had
disappeared completely in the second half of March. Pearson's r for the
correlation between amount of rainfall and INP-8 has a value of 0.45 for
all weeks without snowfall (n = 61) and 0.53 for all weeks with neither
snowfall nor snow on the ground (n = 55). Both correlations are
statistically significant (p < 0.01). There are at least two reasons
for the deviations: first, depending on rain intensity and raindrop size, the
same amount of weekly rainfall can have a very different impact on
aerosolising microorganisms from vegetation (Paul et al., 2004). Second, the
presence and density of IN-active (ice nucleation active) material on surfaces hit by raindrops may
change with season or on shorter timescales. Considering both issues, the
time course of INP-8 mirrors that of rainfall surprisingly well
(Fig. 2).
Potential source regions
Source receptor sensitivity (SRS) fields for situations with > 4
INP-8 m-3 (a) and when INP-8 were < 4 m-3
(b) as derived from FLEXPART. The SRS unit is seconds, which would
result in a mass concentration (kg m-3) at the receptor when multiplied
with an emission flux (kg m-3 s-1) into the model grid cells.
Since emission fluxes are not known for INP-8, SRS values can be
considered as a measure of relative impact that INP emissions from a
particular area would have had on INP concentrations at Birkenes. The
potential influence was strongest from areas shown in red and weakest
from those in white and purple.
We summarised source receptor sensitivity (SRS) fields for situations with
> 4 INP-8 m-3 and when INP-8 were < 4 m-3 in
PM10 (Fig. 3). Higher concentrations of INP-8 were not associated
with additional source areas to those seen when INP-8 were
< 4 m-3. Hence, the higher concentrations of INP-8 were not
transported to Birkenes from specific strong sources afar. The main
difference when INP-8 were > 4 m-3 was a weaker influence from
the north-east (Fennoscandia, Norwegian Sea, Barents Sea, north-western Russia,
Siberia). Air masses from the north-east mainly arrive at Birkenes with high-pressure
systems and bring little or no rain. Large amounts of rain arrive
with cyclones of the North Atlantic storm track. Although high INP-8
concentrations are also associated with enhanced transport from northern
Africa, this transport signal is due only to a few cases and unlikely to
cause the higher INP-8 levels. Furthermore, the Saharan Air Layer
sampled off the western coast of northern Africa on Tenerife over the course of
a year, and analysed by the same method as we used here, was previously found
to contain no more than 1 INP-8 m-3, even during dust storms
(Conen et al., 2015). Overall, there was only a minor difference in the
proportion of influence from land surfaces between situations with higher or
lower values than 4 INP-8 m-3 (48 and 51 %, respectively) and
even smaller differences in land cover type. The small difference in the SRS
fields supports the idea that it is rain and its impact on aerosolising
INP-8 locally that drives temporal variation in INP-8
concentrations at Birkenes.
Size of INP-8
At seven other sites across the Northern Hemisphere, Mason et al. (2016)
found 38 to 90 % of INP-15 collected with a cascade impactor to be
larger than 2.5 µm (mean = 62 %, s.d. = 20 %). In the
present study, INP-8 were equally distributed amongst the fine
(PM2.5) and the coarse fraction (PM10-2.5) of PM10 (Fig. 4).
Such a 50–50 % distribution can be expected, if there is a unimodal,
normal distributed peak of INP-8, which peaks around 2–3 µm
aerodynamic diameter. Some findings support this presumption. Schumacher et
al. (2013) continuously measured the size distribution of
fluorescent biological aerosol particles (FBAP) over 18 months at a site in southern
Finland, 960 km to the east of Birkenes, while also observing a marked decrease in
atmospheric concentrations at times when snow covered the ground. Their
results showed a dominant, often extremely narrow mode between 2.5 and
3.0 µm. Similar observations at a forest site in Colorado revealed
rain-induced increases in FBAP with a peak at 2.0 µm (Schumacher et
al., 2013).
Ice-nucleating particles active at -8 ∘C in PM2.5,
relative to their number in PM10.
Huffman et al. (2013) have demonstrated a close link
between FBAP and INPs for the site in Colorado. They saw rainfall that immediately increased the number of
airborne biological particles with a size of 2–3 µm, while also increasing INP-15. In addition, larger particles
(4–6 µm), comprising INPs,
appeared several hours later and lasted for up to 12 h after rainfall had
ceased. Huffman et al. (2013) were able to identify several IN-active species
from aerosol samples collected during rainfall, including two fungi
previously unknown to be IN-active that produced spores between 1 and
4 µm in geometric size. Strong correlations between FBAP and fungal
spore markers, such as arabitol, strongly supported the notion that most FBAP
aerosolised during rain were of fungal origin (Gosselin et al., 2016).
Weekly concentration of arabitol (red) and mannitol (magenta). The
time courses of INP-8 in PM10 (black; × 5, to fit onto the
same scale) and precipitation (blue) are copied from Fig. 1 to facilitate
direct comparison.
Another important source of FBAP in PM10 is pollen (Manninen et al.,
2014). Pollen from birch, the most abundant deciduous tree around the
Birkenes Observatory, has an aerodynamic diameter of 20 µm
(Efstathiou et al., 2011). Smaller fragments of pollen are generated by
osmotic rupture when pollen grains get wet. These fragments are as IN-active
as intact grains (Pummer et al., 2012). On rainy days their abundance
increases in the fine fraction (Rathnayake et al., 2017). However, we can
exclude a major contribution of pollen-derived INPs, because exposure to
90 ∘C deactivated all INP-8 in 9 of the 10 samples treated
that way and 92 % of INP-8 in the remaining sample
(26 March–2 April 2014). Still, a few heat-resistant INP-8 might have
escaped observation at concentrations below the limit of detection in our
approach (0.08 m-3). If so, they would constitute, on average, 7 % or
less of INP-8 found prior to treatment. The INPs of bacteria and most
fungi are proteins and denatured at this temperature (Pummer et al., 2015).
INPs from pollen or fractured pollen are most likely polysaccharides and would
have remained active after heating to 90 ∘C (Pummer et al., 2012,
2015).
Recently, Wang et al. (2016) described a mechanism that generates airborne
soil organic particles (ASOPs) of submicron size by air bubbles bursting at
the water–air interface of impacted raindrops. Soil organic matter can
harbour large numbers of INP-8 (Schnell and Vali, 1972; Conen et al.,
2011; O'Sullivan et al., 2015; Hill et al., 2016). Therefore, some of the
INP-8 in the fine fraction at Birkenes might be of that kind.
Time series of arabitol and mannitol
Arabitol and mannitol serve as carbohydrate stores in fungal spores. Their
ambient air concentration has been found to correlate well with number
concentrations of airborne fungal spores (Bauer et al., 2008), but not
necessarily with ergosterol (Burshtein et al., 2011), a dominant sterol in
most fungi (Weete et al., 2010). It seems that arabitol and mannitol are
specifically associated with spores released under moist conditions, as occur
in forests during night-time (Zhu et al., 2016). At Birkenes, arabitol and
mannitol had very similar temporal patterns throughout the year (Fig. 5).
Their concentrations were low from January to mid-April, then increased and
remained enhanced throughout summer. During the warmer part of the year, from
mid-May to mid-September, they correlated significantly with INP-8
(mannitol: r = 0.72, p < 0.01; arabitol: r = 0.48,
p < 0.05). These correlations (Fig. 6) support the above-mentioned
notion (Sect. 3.3) that FBAP and INP-8 may to some extent be of fungal
origin, at least during the warmer part of the year. Another hint in this
direction comes from measurements about 300 km north-east of Birkenes.
There, in summer, arabitol and mannitol had a unimodal size distribution
peaking between 2 and 4 µm aerodynamic diameter (Yttri et al.,
2007), which coincides with our interpretation of the 50–50 % distribution
of INP-8 amongst PM2.5 and PM10-2.5. Concentrations of the
fungal spore markers increased towards the end of 3 rather dry weeks in
September and reached their annual maxima with intensive rainfall at the
beginning of October, followed 1 week later by a 7-fold increase in
INP-8. Changes in INP-8 continued to follow those of the fungal
spore markers with a delay of 1 week until the beginning of December. In
December, INP-8 remained elevated whereas, concentrations of arabitol and
mannitol decreased markedly. The fungal spore markers and INP-8 reached
their minimum with snowfall in the last week of the year.
Correlation between INP-8 and the fungal markers mannitol
(a) and arabitol (b) for the time period from 14 May to
24 September 2014 (black circles, regression line and equation are fitted to
these data). Concentrations of INP-8 before and after this period
(crosses) did not correlate with either fungal spore marker.
Assuming 1.2 pg arabitol and 1.7 pg mannitol per fungal spore (Bauer et
al., 2008), we estimate for the period from mid-May to mid-September average
spore concentrations of 4.6 and 5.8×103 m-3. The average
concentration of INP-8 during the same period was 1.6 m-3. If all
INP-8 were spores, there would have been 2.8 or 3.5×10-4 INP-8 per spore, which is in the upper range of values
reported by Morris et al. (2013, Fig. 1) for urediniospores of rusts. However,
spores found in the atmosphere are not only produced by rusts. For example,
Cladosporium species contribute a large proportion of airborne
spores (Maninnen et al., 2014) and their onset of freezing is well below
-25 ∘C (Iannone et al., 2011). At the same time, some fungi
release INP-8 from their mycelium in the form of macromolecules
(Fröhlich-Nowoisky et al., 2015), which are unlikely to contain storage
products, such as arabitol or mannitol.
For the last 3 months of the year, the average INP-8 to spore ratio
was about twice as large as compared to the preceding 4 months. Since the
time course of INP-8 was no longer directly related to that of fungal
spore markers during this period, it might be that the fungal composition
had changed, or that bacteria had become a more important source of
INP-8. The expression of ice nucleation activity in bacteria is
favoured by cold temperatures and nutrient limitation (Nemecek-Marshall et
al., 1993). Hence, when similar numbers of bacteria are aerosolised by the
same amount of rainfall, they likely contribute larger numbers of INP-8
during the cold season than during the warm months. Overall, the relative
contribution of INP-8 from any type of microorganism might have changed
by the end of September, as a result of leaves starting to be shed by
deciduous trees. Decaying leaves provide the substrate for a highly
dynamical succession of interacting fungal and bacterial populations
(Purahong et al., 2016).
Conclusions
Abundant rainfall in the coastal climate of southern Norway drives the near-surface
concentration of INP-8 across all seasons. Concentrations of
INP-8 increase with amounts of rain. Most airborne INP-8 are
probably aerosolised locally through the impact of raindrops onto surfaces
hosting microorganisms that synthesise INPs. Snowfall has no such effect.
When trees are defoliated between October and April, decaying leaf litter on
the ground constitutes a likely INP source. During this time, snow cover on
the ground strongly reduces such INP aerosolisation by rainfall.
Rain-released INP-8 are equally distributed amongst the fine
(PM2.5) and the coarse fraction (PM10-2.5) of PM10.
Sensitivity to heat treatment (90 ∘C) suggests bacterial and
fungal sources and not pollen. The assumption of relevant fungal sources is
supported during the warmer part of the year by some similarities in the
temporal pattern of INP-8 and the fungal spore markers, arabitol and
mannitol. However, major shifts in microbial community composition occur
when leaves are shed in autumn and start to feed a highly dynamical
succession of interacting fungal and bacterial populations. These dynamics
likely also affect the strength and composition of the various sources of
INP-8.
In general terms, we expect similar relations between rainfall and warm-temperature
INPs in other coastal regions with a comparable climate and
ecosystem, such as the Pacific coasts of Canada and Chile, Japan, and New
Zealand. Global warming may lead to shorter periods of snow cover on the
ground and a greater proportion of precipitation falling as rain instead of
snow. These changes would probably result in larger airborne concentrations
of INP-8 during the cold season. Whether they have an effect on cloud
development in these regions remains an interesting question for further
studies.