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Temporal and Spatial Variability of Volatile Organic Compounds in the Forest Atmosphere

International Journal of

Environmental Research

and Public Health

Article

Temporal and Spatial Variability of Volatile Organic

Compounds in the Forest Atmosphere

Francesco Meneguzzo 1,2,* , Lorenzo Albanese 1, Giorgio Bartolini 3 and Federica Zabini 1,*

1 Institute for Bioeconomy, National Research Council, 10 Via Madonna del Piano,

I-50019 Sesto Fiorentino (FI), Italy; lorenzo.albanese@ibe.cnr.it

2 “Fiorenzo Gei” Scientiﬁc Committee, Italian Alpine Club, 2 Via del Mezzetta, I-50135 Firenze (FI), Italy

3 Laboratory of Monitoring and Environmental Modelling for the Sustainable Development (LaMMA

Consortium), Via Madonna del Piano 10, 50019 Sesto Fiorentino, Italy; bartolini@lamma.rete.toscana.it

* Correspondence: francesco.meneguzzo@ibe.cnr.it (F.M.); federica.zabini@ibe.cnr.it (F.Z.);

Tel.: +39-392-985-0002 (F.M.); +39-333-379-2947 (F.Z.)

Received: 20 November 2019; Accepted: 3 December 2019; Published: 5 December 2019

Abstract: The healing eﬀects of the forest are increasingly being valued for their contribution to

human psychological and physiological health, motivating further advances aimed at improving

knowledge of relevant forest resources. Biogenic volatile organic compounds, emitted by the plants

and accumulating in the forest atmosphere, are essential contributors to the healing eﬀects of the

forest, and represent the focus of this study. Using a photoionization detector, we investigated the

high frequency variability, in time and space, of the concentration of total volatile organic compounds

on a hilly site as well as along forest paths and long hiking trails in the Italian northern Apennines. The

scale of concentration variability was found to be comparable to absolute concentration levels within

time scales of less than one hour and spatial scales of several hundred meters. During daylight hours,

on clear and calm days, the concentration peaked from noon to early afternoon, followed by early

morning, with the lowest levels in the late afternoon. These results were related to meteorological

variables including the atmospheric vertical stability proﬁle. Moreover, preliminary evidence pointed

to higher concentrations of volatile organic compounds in forests dominated by conifer trees in

comparison to pure beech forests.

Keywords: bioactive compounds; forest air; forest bathing; forest therapy; hiking trails; human

health; monoterpenes; stress; volatile organic compounds

1. Introduction

In recent years, attention has continued to grow with respect to the use of the forest environment

for health purposes [1]. Plenty of recent evidence supports the value attributed to forest bathing, or

forest therapy, derived from the Japanese Shinrin-Yoku, a kind of forest recreation traditionally practiced

for improving physical and mental health and as a remedy for stress [2].

Signiﬁcant positive eﬀects on mental health, especially in people with depressive tendencies,

were demonstrated by psychological analyses and physiological measurements, showing remarkable

improvements in mood and depressive symptoms [3–5], a decrease in anxiety and stress levels [6–8],

and a decreased risk of psychosocial stress-related diseases [9–11]. On the physiological side, the forest

environment showed anti-hypertensive eﬀects [10,12,13], promoted the regularization of the heart rate

variability [14–16], increased the numerosity and activity of human natural killer cells [17–19], and

induced the decrease of the blood glucose levels in diabetic patients [20].

Based on the above-mentioned health eﬀects, forest therapy has been attributed a speciﬁc

role in medical prevention. Healthcare programs based on forest therapy have been developed in

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www.mdpi.com/journal/ijerph

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some countries [21] and have recently been recommended on a large scale, with a sound economic

foundation [22].

Among several factors able to trigger physiological activation in the forest environment, the

inhalation of aromatic volatile substances, i.e., biogenic volatile organic compounds (BVOCs), plays an

important role [17]. BVOCs, as low-molecular-weight compounds [23]„ are emitted by plant parts

above and below the ground, as well as by leaf litter, soil microbes, and insects, and show important

functions for protection, defense, and communication among plants as well as between plants and

other organisms [24]. All plant organs from ﬂowers to roots can generate and release BVOCs [25], with

leaves generally producing the highest emission rates [26].

Volatile terpenes represent most of the BVOC emissions in the forest environment, such as

isoprene (which accounts for about 50% of the global emitted BVOCs per year), and monoterpenes

(MTs, consisting of two isoprene units and accounting for about 15%) [27]. Thus, isoprene and MTs

represent the major components of forest aerosols [26].

Based on decades of studies, reliable catalogues of the BVOC emission potential of leaves and

needles of major European forest tree species are nowadays available. Notably, trees able to store MTs,

such as conifer species, are not necessarily the highest potential emitters, with deciduous trees typical

of mountainous forests in European temperate areas, such as beech (Fagus sylvatica) and chestnut

(Castanea sativa), potentially greatly exceeding widespread conifer species such as Norway spruce (Picea

abies) and silver ﬁr (Abies alba) [28]. However, some studies showed that conifers can be important

emitters of their respective typical MTs, among which α-pinene and d-limonene often stand out, which

are endowed with recognized and important biological activities [29].

Beyond the large diﬀerences among forest tree species, the study of the variability of BVOC

emission rates is hindered by their high reactivity with other compounds in the atmosphere, and by

the high variability of biosynthesis and emission mechanisms, leading to remarkable intraspeciﬁc

diﬀerences in terpene emission with regard to both total emissions and chemical proﬁle [30]. Emission

rates from leaves depend on several factors, such as physiological (age and developmental stage of plant)

and physicochemical aspects (i.e., related to temperature, stomatal openness, and leaf structure) [31].

Temperature and light (radiation) were shown to be key environmental mechanisms for the

synthesis and emission of BVOCs. Generally, isoprene emission is high dependent on light as well

as on temperature due to its high volatility [31]. MT emission may show diﬀerent sensitivity to light

and temperature, also depending on the presence or absence of storage structures [32]. In plants with

BVOC storage compartments, the emissions are basically temperature-dependent because temperature

is able to volatilize compounds from stored pools, whereas in plants not storing BVOCs the emission

rate is light and temperature-dependent [33,34]. Temperature variability aﬀects also the VOC ﬂuxes

from the forest ﬂoor [35].

A recent study performed by Korea’s National Center for Forest Therapy focused on the variability

of BVOCs concentration in the atmosphere of a Pinus densiﬂora forest, on a ﬁxed site, during daylight

hours (one-hour measurements starting at 08:00 am, 12:00 pm, and 17:00 pm), and once a month for a

year [36]. The study was motivated by the consideration of BVOCs as an important resource in forest

therapy due to their wide-spectrum healing eﬀects, and was carried out by means of absorbent tubes

and subsequent desorption and gas chromatographic analysis.

A remarkable seasonal variability was found, with the concentration of total BVOCs being highest

in summer, followed by spring and fall, and lowest in winter. In summer, the relative concentration of

α-pinene was also the highest, showing that not only total BVOCs but also individual components may

change seasonally. On a daily basis, BVOC concentrations were found to increase from 08:00–09:00 am

to 12:00–13:00 pm, and again, marginally, up to 17:00 pm, in contrast to previous studies which found

higher concentrations at sunrise and sunset. However, admittedly, the discrete sampling prevented

drawing deﬁnitive conclusions.

This study presents the results of a few high-frequency monitoring campaigns of total volatile

organic compound (TVOC) concentrations both on ﬁxed sites and along paths (a forest path and

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few hiking trails) far from anthropogenic sources, with each campaign carried out for several hours

during daylight. Beyond the representativeness of the measurements of TVOCs with regard to

BVOCs, such relative remoteness was deemed to minimize the reaction of terpenes with anthropogenic

pollutants that, in contaminated environments such as urban forests, might enhance photochemical

pollution [30], possibly oﬀsetting the BVOC-related health beneﬁts. No other previous studies

investigated the variability of the concentration of TVOCs or BVOCs, in the forest air with such

temporal and spatial detail, let alone along long paths (tens of km), spanning diﬀerent elevations,

climates, and forest compositions.

2. Materials and Methods

2.1. Measurement of Volatile Organic Compounds

TVOCs in the forest atmosphere were measured by means of a portable (0.72 kg) photoionization

detector (PID, model Tiger VOC detector, Ion Science Ltd., Fowlmere, Royston, UK), with detection

limits from 0.001 ppm (1 ppb) to 20,000 ppb. The PID was equipped with a pump, aspiring the

ambient air at a rate of 220 mL/min, and an ultraviolet, 10.6 eV lamp allowing the ionization of organic

substances in the aspired air, including all the MTs found in BVOCs. The resulting electric current

ﬂowing between two electrodes was measured and ampliﬁed, and transformed into a concentration

level of the ionized substance or group of substances.

Factory calibration was performed at the temperature of 21.5 ± 0.1 ◦C and atmospheric pressure

with respect to the substance isobutylene, with an estimated measurement uncertainty of ±2%. The

concentration of other substances was derived after the application of a response factor that, for TVOC,

was equal to 1. While practically immediate, this detection method did not allow the identiﬁcation

of single compounds in TVOCs, which would require a gas chromatograph. This issue is discussed

further in Section 4.

2.2. Study Sites and Weather Stations

Figure 1a shows the location of the study sites in a wide geographical context, across Tuscany and

the Emilia-Romagna regions, Italy, labeled as S1 (hilly site), S2 (forest path), and H1 and H2 (hiking

trails). The considered weather stations (W1 to W9) are represented too. The study areas are shown

in detail in Figure 1b–e, with the forest path (S2) shown in yellow, and the hiking trails (H1 and H2)

represented by red and blue lines.

Table 1 shows the list of the study sites and the weather stations, along with the respective

geographical coordinates (for weather stations), elevation, and data collected.

Table 1. List of study sites and weather stations.

Type

Lat

Lon

Elevation

Data

S1 1

Hilly site

43◦41 21.16

10◦50 08.38

61 m a.s.l.

TVOC

Weather station 43◦40 48.00 N 10◦53 00.40 E

117 m a.s.l.

W, GR 4

Weather station 43◦40 48.00 N 10◦49 00.80 E

102 m a.s.l.

S2 2

Forest path

960–1150 m a.s.l.

TVOC

H1 2

Hiking trail

960–1855 m a.s.l.

TVOC

Weather station 44◦01 12.00 N 11◦01 00.80 E

950 m a.s.l.

Weather station 44◦02 24.00 N 10◦55 00.20 E

785 m a.s.l.

Weather station 44◦07 48.00 N 10◦46 00.80 E

1716 m a.s.l.

T, W, RH

Weather station 44◦07 48.00 N 10◦44 00.40 E

1000 m a.s.l.

H2 3

Hiking trail

1312–1816 m a.s.l.

TVOC

Weather station 44◦12 00.00 N 10◦29 00.40 E

1637 m a.s.l.

T, W, GR

Weather station 44◦12 36.00 N 10◦27 00.00 E

1297 m a.s.l.

Weather station 44◦16 55.56 N 10◦24 00.10 E

2057 m a.s.l.

T, W

1 Meteorological data from weather stations W1 and W2. 2 Meteorological data from weather stations W3, W4,

W5, and W6. 3 Meteorological data from weather stations W7, W8, and W9. 4 Meteorological data abbreviations

and units: T, air temperature 2 m above ground (◦C); W, wind intensity 10 m above ground (ms−1); RH, relative

humidity 2 m above ground (%); GR, global radiation (Wm−2); TVOC, total volatile organic compound (mg/kg).

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All weather data were collected every 15 min and consisted of the respective averages over

the previous 15 min. The weather stations W1 to W8 belonged to the monitoring network of the

Regional Functional Center for Weather—Hydrological Monitoring, Tuscany, Italy (http://cfr.toscana.it/).

Weather station W9 belonged to the monitoring network of the “Reggio Emilia Meteo” association

(http://www.reggioemiliameteo.it/), and the respective data (temperature and wind) were retrieved

from the public web site.

(a)

(b)

(c)

Figure 1. Cont.

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(d)

(e)

Figure 1. (a) Study sites (S1, S2, H1, and H2), and weather stations (W1 to W9), in a wide geographical

context (central and northern Tuscany, Italy). (b) Detail over the (hilly) study site S1. (c) Detail over

the study site S2, with the forest path represented by a yellow line. (d) Detail over the study site H1.

(e) Detail over the study site H2. The hiking trails H1 and H2 are represented by red and blue lines.

2.3. TVOC, Geographical, and Meteorological Data: Measurement, Logging and Merging

The measurement sessions on the ﬁxed site S1 were carried out with PID pump placed 1.2 ± 0.1 m

above the ground, with such height corresponding approximately to the height of the nose of a 1.75-m

tall person sitting on a chair. The measurement sessions along pathways (S2, H1, and H2) were carried

out with the PID ﬁxed on the backpack. The pump was again placed 1.2 ± 0.1 m above the ground,

and the paths were always traveled on foot, in order to avoid any contamination from engine exhaust

gases. However, most of the routes could not be traveled by other means.

The PID logged data every 2 s, with each data string consisting of the time of measurement and

TVOC concentration level in ppm unit (mg/kg). For each measurement session, the lowest detected

concentration (which could be positive or negative, due to the factory calibration used), was subtracted

from all the other data, in order to remove, as much as possible, background TVOC concentration

level. Such background level likely included BVOCs too, and thus resulting TVOC concentration levels

could be considered as lower estimates of the actual BVOC concentration levels, especially due to the

remoteness of the considered sites from any anthropogenic source.

While in principle changes of the levels of anthropogenic VOCs during time spans of a few hours

could not be ruled out, for example due to changes in the atmospheric vertical stability or to changes

in the emission rates from anthropogenic sources, the above-mentioned remoteness should keep such

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uncertainty at comparatively low levels. This topic is further discussed in Section 4. Finally, since

this study aimed at a preliminary assessment of the relative variability in time and space of BVOC

concentration levels within the forest atmosphere, the accurate assessment of the respective absolute

concentration levels remains outside the scope.

Limited to the measurements along pathways, continuous geographic localization was performed

by means of Global Positioning System (GPS) software installed in a commercial smartphone (Open

GPX Tracker, https://apps.apple.com/it/app/open-gpx-tracker/id984503772), with data logging every

7 s, including the time of measurement, latitude, and longitude. The height above sea level (a.s.l.)

was assigned to each geographical point, based on the dataset of the National Aeronautics and Space

Administration, Shuttle Radar Topography Mission (NASA’s SRTM), 30-m horizontal resolution, by

means of an online conversion software (GPS Visualizer, https://www.gpsvisualizer.com/convert_input).

The PID and the smartphone were synchronized, and then TVOC and geographical data were merged

based on the respective measurement times, with TVOC data interpolated to the time points of the

GPS data.

In order to assign to each TVOC data point, at any time, a complete set of meteorological data

(temperature, global radiation, and wind intensity), the data collected at the weather stations were

interpolated as follows. At local elevations below or above the range of elevations of the considered

stations, the air temperature measured at the nearest weather station was interpolated based on the local

elevation, according to the standard vertical gradient in the lower troposphere of −0.6 ◦C/100 m [37].

Otherwise, a linear interpolation to the local elevation was performed, based on data collected at the

weather stations located at the closest elevations below and above the local one.

The wind intensity was linearly interpolated to the local elevation, based on two of the weather

stations located at elevations closest the local one. Global radiation data were available only at a single

weather station for each study site. However, due to the observed low-level cloudiness around the

ridge along the H1 hiking trail, the global radiation data at elevations above 1600 m a.s.l. were corrected

to random levels between 0 and 100 Wm−2—a range representative of cloudy conditions—whenever

the relative humidity at the weather station W5 was at the level of 95% or above. While this was a

somehow arbitrary choice, adopted for representation purposes, the correction was imposed by the

relative remoteness of the weather station W5 (measuring the global radiation), its location far below

the mountain ridge, and the local character of the cloudiness over the ridge itself. Moreover, knowing

the exact level of the radiation below 100 Wm−2 was practically useless for the purposes of this study.

3. Results

3.1. Hilly Site

3.1.1. Clear and Calm Days

Figure 2a–c shows TVOC concentration and weather data series for the hilly site, labeled as site S1

in Table 1, during days with generally clear skies, low wind (average wind intensity over 15 min lower

than 3 m/s), and relatively high temperatures. TVOC concentration, temperature, and global radiation

are shown in Figure 2a–c, respectively.

The relative changes of TVOC concentration, during any given day, spanned from 0.5 to more

than 0.9 ppm, i.e., around the magnitude of the highest concentration levels commonly observed in the

forest air [29]. During any given day, TVOC relative concentration appeared to peak during the time

period 13:00–14:00 pm to 16:00 pm solar time, seemingly following the peak air temperature which lags

behind peak radiation rather than global radiation itself. However, dependence of TVOC concentration

on radiation could not be ruled out, for example due to the accumulation and persistence of MTs in

the lower atmosphere. Forest in site S1 was locally dominated by both evergreen trees (storing MTs)

such as cypress and eucalyptus and deciduous trees such as oak and poplar, suggesting dependence

on both temperature and radiation [32]. However, looking at diﬀerent days, no evidence arose with

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respect to a monotonic relationship between the maximum amplitude of the daily concentration cycle

and the peak temperature.

(a)

(b)

(c)

Figure 2. Data on site S1 during generally clear and calm days. (a) Total volatile organic compound

(TVOC) concentration; (b) Air temperature; (c) Global radiation.

Radiation played a more remarkable role in late afternoon (approximately, after 16:00 pm), when

air temperature decreased slowly and was still relatively higher than in the morning, while TVOC

concentration dropped much faster than the respective rate of increase observed in the morning. Likely,

emissions from deciduous trees dropped quickly with the vanishing radiation. This could be conﬁrmed

based on the event that occurred on 1 September 2019, when the sudden drop in TVOC concentration,

starting around 15:30 pm, followed the fast decrease of global radiation (related to a sudden storm

approaching the site), with a short delay (about 30 min). The air temperature dropped too, down

to approximately the levels shown in the same time period during the days of 28 September and

6 October, when TVOC concentrations did not drop signiﬁcantly.

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Another important factor contributing to the falling concentration in late afternoon might be the

eﬀect of the lowering of radiation levels on the atmospheric vertical stability, especially during clear

and calm days, and thus on the diﬀusivity of aerial substances down to the ground. This topic will be

discussed further in Section 4.

Finally, on 28 September 2019, the initial TVOC concentrations (around 07:00 am) were relatively

higher than subsequent levels, until about 10:00 am, despite lower radiation and air temperature.

This behavior could be suggestive of some relationship between TVOC concentrations and other

atmospheric properties, such as the atmospheric vertical stability, which will be discussed further in

Section 4.

3.1.2. Other Days

Figure 3a–d shows TVOC concentration and weather data series for the hilly site, labeled

as site S1 in Table 1, during days with generally cloudy skies, lower temperatures, or relatively

sustained wind. TVOC concentration, temperature, global radiation, and wind intensity are shown in

Figure 3a–d, respectively.

The relative changes of TVOC concentration, during any given day, did not exceed 0.5 ppm, i.e.,

substantially less than on clear and calm days. The global radiation was not much lower than in the

clear days, although generally more irregular. The air temperature was generally lower, which—along

with frequent drops in radiation—could explain the generally lower levels of the amplitude of TVOC

concentration cycles.

On 24 August 2019, the delayed peak in the air temperature, around 16:00 pm, was associated

with the peak in TVOC concentration, which could have been favored also by the decreasing wind

intensity and the relatively high radiation levels. On 9 September, the sudden radiation drops after

about 13:00 pm and the simultaneous increase in the wind intensity could have been the drivers of

TVOC concentration decline after a weak peak around 10:00 am, when the wind was low and the

radiation already suﬃciently high.

Over two days, 9 September and 15 September, with measurements beginning early enough

in the morning when there was suﬃcient radiation (contrary to other days) and the wind was low,

TVOC concentration was higher in the early morning (07:00–08:00 am) than in the following few

hours. Again, this evidence possibly points to a relationship between TVOC concentration and the

vertical atmospheric stability, which was already noted in Section 3.1.1 and will be discussed further in

Section 4.

On the other hand, TVOC concentrations appeared to fall generally less steeply in the afternoon

than in the clear and calm days considered in Section 3.1.1. Since the solar radiation aﬀects the

atmospheric vertical stability more substantially during clear and calm days, this behavior could be

again suggestive of an important role played by the atmospheric vertical stability. This topic will be

discussed further in Section 4.

(a)

Figure 3. Cont.

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(b)

(c)

(d)

Figure 3. Data on site S1 during generally cloudy, colder, or windy days. (a) TVOC concentration;

(b) Air temperature; (c) Global radiation; (d) Wind intensity.

3.2. Forest Path

Figure 4a–d shows TVOC concentration and weather data series for the forest path, labeled as

site S2 in Table 1, measured on 11 September 2019. Figure 4e–h shows the same quantities for site S2,

measured on 5 October 2019.

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(a)

(e)

(b)

(f)

(c)

(g)

(d)

(h)

Figure 4. Data along forest path S2 on 11 September 2019. (a) Elevation and TVOC concentration;

(b) Air temperature; (c) Global radiation; (d) Wind intensity. On 5 October 2019: (e) Elevation and

TVOC concentration; (f) Air temperature; (g) Global radiation; (h) Wind intensity.

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Based on weather data, shown in Figure 4b–d, 11 September 2019 was a clear and calm day,

with very low wind; air temperatures were in the range 16 to 23 ◦C. The cyclical trend of TVOC

concentration, with local peaks around the lowest elevation of the forest path, and local minimums at

the highest part of the path, points to a remarkable spatial variability, with a maximum amplitude

around 0.4 ppm. Such variability could be related to either the air temperature (decreasing with the

elevation at any ﬁxed time), or the plant species and status, soil emissions, and so on.

The above-mentioned peaks occurred at very diﬀerent levels. In particular, TVOC concentration

peaks were substantially higher in the early morning (before 09:00 am) and just after 12:00 pm, than

around 10:00 am, 14:30 pm, and 16:00 pm. Similar to the behavior observed in Section 3.1, temperature

could have driven up TVOC emissions and concentrations during the hottest few hours of the day,

while the radiation-driven atmospheric vertical stability could have aﬀected TVOC concentration

levels near the ground in early morning (increase) and late afternoon (decrease).

Based on weather data, shown in Figure 4f–h, 5 October 2019, was a calm day with very low

wind, but with alternation of cloudiness and sunny spells, as apparent in the radiation data. The air

temperatures ranged from about 13 to 17 ◦C and no rain was observed during the day.

A cyclical trend of TVOC concentration appeared again in Figure 4e, qualitatively very similar

to that observed in Figure 4a, with local peaks around the lowest elevation of the forest path, local

minimums at the highest part of the path, and maximum amplitude around 0.55 ppm. Such greater

amplitude could have been due to the wild changes in radiation.

The absolute peak in TVOC concentration was again observed in early afternoon, in particular

between 12:40 and 14:00 pm, during a prolonged stop at the lowest site of the route. Interestingly,

TVOC concentration increased by more than 0.25 ppm since the arrival at the lowest site, possibly

following the sudden spike in radiation, with air temperatures around the peak of day. The second

peak in radiation occurred around the highest elevation site of the route (around 14:30 pm), and could

have helped to retain a relatively high concentration level. The subsequent fast drop in radiation could

explain the substantial absence of further peaks at the lowest site.

3.3. Hiking Trails

Figure 5a–e shows TVOC concentration (both superimposed on a topographic map and as a chart)

and weather data series for the uphill part of the hiking trail labeled as H1 in Table 1, as measured on

12 October 2019. The lowest TVOC concentration level in Figure 5b is above zero because the oﬀset

was computed over the whole day, i.e., over the entire hiking trail, including the downhill part, which

is described below. The ﬁrst part of the route, labeled as A in Figure 5b, coincided with the forest path

(site S2 in Table 1) analyzed in Section 3.2.

TVOC concentration increased by nearly 0.6 ppm along part A of the route (forest path, site S2 in

Table 1, with dominance of chestnut, ash, black pine, and silver ﬁr trees), approximately from 09:00 to

09:45 am, which occurred with low wind, relatively high air temperatures, and moderate radiation.

This situation could have mimicked early morning conditions in summer.

Along part B of the route, steeply rising from about 1150 to 1450 m a.s.l., and mostly dominated

by beech and silver ﬁr trees, TVOC concentration remained at comparatively high levels. From

approximately 09:45 to 10:30 am, the global radiation was still moderate, the air temperature decreased

by about 3 ◦C, and the wind intensity was still low, similarly to part A of the route. The subsequent

small local peak in TVOC concentration, along part C of the route, occurred along with a local minimum

of both radiation and air temperature, possibly reinforcing the hypothesis that early morning-like

vertical atmospheric stability could favor relatively high TVOC concentrations near the ground. This

hypothesis will be discussed further in Section 4. In addition, the change in the composition of the

forest vegetation, with beech becoming dominant over ﬁr trees, could have played a role.

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(a)

(b)

(c)

(d)

Figure 5. Cont.

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(e)

Figure 5. Data along the uphill part of the hiking trail H1 on 12 October 2019. (a) TVOC concentration

classes on a topographical map (red, 0–0.225 ppm; yellow, 0.225–0.450 ppm; blue, 0.450–0.675 ppm;

green, 0.675–0.892 ppm), with the red colored house representing the site “Pian dei Termini”, and the

symbols with blue shield surmounted by an eagle representing mountain refuges, managed by the

Italian Alpine Club; (b) Elevation and TVOC concentration; (c) Air temperature; (d) Global radiation;

(e) Wind intensity.

Along parts D and E of the route, with elevation eventually reaching about 1600 m a.s.l. and the

trail emerging outside a pure beech forest and reaching a mountain grassland, TVOC concentration

gradually dropped to a minimum. During these parts of the route (from around 10:45 to 11:45 am),

the wind intensity increased as the mountain ridge was approached, the radiation reached the daily

peak (over 600 Wm−2), and the air temperature changed slightly. Although the relatively high

radiation levels should have favored the BVOC emissions from beeches, the neutral to unstable vertical

atmospheric proﬁle could have diluted the VOCs across a deeper atmospheric layer, thus lowering

TVOC concentrations near the ground. Moreover, the change from mixed beech–ﬁr tree forest to pure

beech forest could have contributed to the observed drop under the speciﬁc meteorological conditions.

The absolute peak in TVOC concentration, observed along part F of the route (from around 12:00

to 12:45 pm), is harder to explain. Most of the route crossed a mountain grassland, only occasionally

reentering the forest; air temperature did not change remarkably, while radiation oscillated wildly

between nearly zero (ridge inside low clouds) and almost 500 Wm−2. Notably, the southwesterly

wind intensity increased up to the daily maximum of 5 ms−1, which might suggest the advection of

BVOCs from the nearby forest and the respective accumulation near the ground on the upwind side

of the ridge. The same factors could also explain why TVOC concentration dropped by only about

0.3 ppm, well below what one could have expected, along part G of the route (12:45 to 13:45 pm),

entirely developing around the ridge and on mountain grasslands, with very low radiation and air

temperatures at the da− ily minimum (around 7 ◦C).

Figure 6a–e shows TVOC concentration (both superimposed on a topographic map and represented

as a chart along with the local elevation) and weather data series for the downhill part of the hiking

trail labeled as H1 in Table 1, again measured on 12 October 2019. The latter part of this route was

slightly diﬀerent from the uphill path, while eventually getting to the same site, and is labeled with a

diﬀerent letter (H).

−

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(a)

(b)

(c)

(d)

Figure 6. Cont.

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(e)

Figure 6. Data along the downhill part of the hiking trail H1 on 12 October 2019. (a) TVOC concentration

classes on a topographical map (red, 0–0.225 ppm; yellow, 0.225–0.450 ppm; blue, 0.450–0.675 ppm;

green, 0.675–0.892 ppm), with the red colored house representing the site “Pian dei Termini”, and the

symbols with blue shield surmounted by an eagle representing mountain refuges, managed by the

Italian Alpine Club; (b) Elevation and TVOC concentration; (c) Air temperature; (d) Global radiation;

(e) Wind intensity.

TVOC concentrations along most of the downhill route were much lower than along the uphill

route, which is apparent after comparing the maps in Figures 5a and 6a. This comes as little surprise

because air temperatures were generally lower and global radiation even more so due to increased

cloudiness and the progression of time in the afternoon. The lower part of the downhill route (parts E,

D+C, and H in Figure 6b) could have been deeply aﬀected by the changed conditions, with TVOC

concentration levels lower by 0.25 to 0.45 ppm in comparison with the uphill route.

The absolute minimum in TVOC concentration levels in part F of the downhill route shown in

Figure 6b and corresponding to the red colored tags in Figure 6a is especially suggestive. Such levels

were as much as nearly 0.9 ppm lower than the levels observed along the same part of the route just 3 h

earlier. Indeed, this part crossed mainly mountain grasslands, and most of observed VOCs were likely

to be the result of the advection from the nearby forest. With lower radiation and somewhat lower

wind intensity, likely both BVOC emissions from forest trees and the respective advection decreased,

resulting in remarkably lower TVOC concentrations.

Figure 7a–e shows TVOC concentration, both superimposed on a topographic map and represented

as a chart along with the local elevation, and weather data series for the ring-shaped hiking trail labeled

as H2 in Table 1, measured on 29 September 2019.

(a)

Figure 7. Cont.

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(b)

(c)

(d)

(e)

Figure 7. Data along the hiking trail H2 on 29 September 2019. (a) TVOC concentration classes

on a topographical map (red, 0–0.194 ppm; yellow, 0.194–0.388 ppm; blue, 0.388–0.582 ppm; green,

0.582–0.776 ppm), with the square symbol with white background representing the “Segheria” refuge,

managed by the Tuscan-Emilian Apennine National Park, and the symbol with blue shield surmounted

by an eagle representing the “C. Battisti” refuge, managed by the Italian Alpine Club; (b) Elevation and

TVOC concentration; (c) Air temperature; (d) Global radiation; (e) Wind intensity.

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TVOC concentration levels oscillated with a maximum amplitude greater than 0.75 ppm along

the ring-shaped route. The highest peak occurred along the part of the route labeled as A in Figure 7b,

in early morning (08:00 to 08:40 am) at elevations of 1400 to 1550 m a.s.l., in a mixed beech–ﬁr trees

forest with both silver ﬁrs and Douglas ﬁrs. Weather conditions were characterized by moderate global

radiation (300–400 Wm−2), relatively low temperature (9–11 ◦C), and wind intensity (3 to 4.5 ms−1),

likely leading to a shallow neutral to unstable vertical atmospheric proﬁle.

Subsequently, part B of the route (08:45 to 10:15 am) developed across mountain grasslands at

higher elevations (from more than 1800 to about 1750 m a.s.l.), with lower temperatures (about 8 ◦C),

lower radiation levels (200–300 Wm−2), and stronger wind (up to 5.5 ms−1). TVOC concentration levels

dropped to a prolonged absolute minimum, starting from the ridge and further along the leeward

side (the wind was blowing from the south-west). Likely, no eﬀective advection of VOCs occurred

from forests located at least 200 m below the ridge, and constituted (on the windward side) by pure

beech stands.

Along part C (10:15 to 11:30 am) at elevations between 1650 and 1750 m a.s.l., alternately crossing

grasslands and forest stands with both beech and ﬁr trees, TVOC concentrations gradually increased,

eventually by nearly as much as 0.6 ppm, possibly in response to both the presence of tree vegetation

and increased radiation, with the latter reaching about 500 Wm−2. At about 11:30 am–12:30 pm (part

D), TVOC concentration measurements were taken at a ﬁxed point (“C. Battisti” refuge, managed by

the Italian Alpine Club) at the elevation of 1765 m a.s.l., immersed in a mixed beech–ﬁr tree forest.

TVOC concentrations initially increased by further 0.1 ppm, later dropping steeply by as much as

0.45 ppm. The reason of such decline in TVOC concentration may have been the trend in radiation,

initially increasing up to more than 700 Wm−2 and later dropping to an average of 350 Wm−2.

During part E of the route (12:30 to 12:50 pm), developed on the ridge covered by a grassland at

elevations around 1780 m a.s.l., TVOC concentrations remained stationary around a local minimum.

Later, they increased remarkably by about 0.25 ppm at the local peak during the descent across a

historic forest (“Abetina Reale”) dominated by silver ﬁr trees, along with beeches and Norway spruce

(Part F, 12:50 to 13:40 pm), down to about 1400 m a.s.l. (location of the “Segheria” refuge, managed by

the Tuscan-Emilian Apennine National Park). While slightly stronger radiation (up to about 440 Wm−2)

and relatively higher temperature (up to about 12 ◦C) could not be ruled out, the forest vegetation

was likely the main driver for local BVOC emissions and, consequently, increased concentrations near

the ground.

Finally, a forest path crossed a pure beech forest in parts G and H of the route (ascent to the ridge

at the elevation of 1570 m a.s.l., and descent to the starting point of the trail, respectively). Decreasing

radiation levels or the forest composition, or both, could have contributed to relatively lower TVOC

concentrations (about 0.2 ppm below the local peak observed in the “Abetina Reale” forest).

4. Discussion

The meaningfulness of this study and the related ﬁndings relies upon the representativeness

of TVOC concentrations measured by means of a PID with respect to the biogenic components

(BVOC). Since the components of the detected TVOCs were not analyzed in any study sites and

paths, in principle their origin was unknown, i.e., they could be either biogenic or anthropogenic, or

both. However, the remoteness of the areas into consideration from anthropogenic sources, as well

as the adoption of a variable oﬀset concentration level equal to the absolute minimum during any

measurement day, with respect to which all the other data were referred, should have minimized the

chance of substantial contributions of anthropogenic sources to reported TVOC concentration data.

Based on the above, in the following, unless explicitly speciﬁed, the volatile organic compounds under

consideration will be referred to as BVOCs.

The ﬁrst and basic ﬁndings of this study concerned the remarkable variability of BVOC

concentrations in time and space, both on ﬁxed sites and along paths, as well as in diﬀerent environments,

i.e., low hill, mid-mountain sites and mountain sites up to over the upper limit of tree vegetation.

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Indeed, within the same day, relative changes of BVOC concentration commonly exceeded 0.5 ppm,

often even reaching levels as high as 0.9 ppm, on the order of magnitude of the highest concentration

levels observed in the forest air, i.e., around 1 ppm [29]. Such changes occurred within time scales as

short as a few tens of minutes, and within distances of the order of several hundred meters along paths

and hiking trails.

The takeaway message from these ﬁndings is that, as far as BVOCs are considered an essential

resource contributing to the forest healing eﬀects, forest therapists and forest bathers should carefully

choose the right times and forest sites and paths even on clear and calm days. Hikers could incorporate

this information into their walking plans in order to beneﬁt from BVOC inhalation along with the

advantages derived from the physical exercise.

Building a comprehensive quantitative model for BVOC concentration as a function of time of the

day and meteorological data, even on a single site and for clear and calm days, would require much

more extensive and continuous measurements. As well, the seasonality of emission rates from plants

and soil should be included, in turn depending on the speciﬁc forest composition. The structure and

the hourly evolution of the atmospheric boundary layer, including its vertical stratiﬁcation, should be

accurately represented too. The climatology of BVOC concentrations along a path would be even more

challenging, due to changing forest composition and exposure of the path. On the other hand, mapping

BVOC concentration near the ground is just in its infancy, and the road ahead is still very long.

However, some insight could be gained, limited to a single day and on a ﬁxed site. Based on

data collected on site S1 during 28 September 2019, shown in Figure 2a–e and endowed with the

largest daily coverage, the series of 30-min average concentrations of volatile organic compounds was

linearly regressed against air temperature and global radiation. Such regression was carried out both

during the whole period of measurements, and separately for the morning (07:30 am to 12:30 pm) and

afternoon (12:30 to 20:30 pm). The results are shown in Figure 8.

Figure 8. Observed and modeled concentration of volatile organic compounds on site S1 on 28 September

2019. The black line (TVOC—observed) represents the observed concentration. The gray line (TVOC—all

day) represents the result of multiple regression over the whole period of measurements. The green

line (TVOC—morning + afternoon) represents the result with regressions performed separately for

morning and afternoon.

Apparently, the likely, subtle eﬀects produced by the lowest radiation levels in early morning

and late afternoon were represented much more accurately by the separate regressions performed for

morning and afternoon. In addition, the peak concentration, observed around 15:00 pm, was better

represented too, although marginally.

−

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Equations (1) and (2) show the regression equations for morning and afternoon, respectively:

TVOC = −1.14 + 0.09·T − 0.0005·R,

(1)

TVOC = −2.2−6 + 0.11·T + 0.0005·R,

(2)

where TVOC is concentration (ppm), T is temperature (◦C), and R is radiation (Wm−2). −

Equations (1) and (2) explained 82% and 97% of the variance, respectively, and were both signiﬁcant

at the 1% level, based on the F statistics. While the dependence of concentration on temperature was

quite similar, the dependence on radiation was opposite, being negative in the morning and positive

in the afternoon. Likely, this reﬂects the fact that temperature was the main forcing for emissions

from plants [33,34], as well as from soil [35], while radiation drove the evolution of the atmospheric

boundary layer [38]. The following is a preliminary explanation of these results.

In the morning, temperature rises rapidly, stimulating higher emissions, while the increase in

radiation deepens the ground-based boundary layer, through which the emitted compounds are

diluted, thus counteracting the eﬀect of increasing emissions with regard to ground concentration.

In early morning, the shallow boundary layer leads to relatively higher concentration despite the low

emission levels. In the afternoon, declining radiation eventually determines a ground-based stable

atmospheric layer, in turn surmounted by a residual mixing layer [38], thus hindering the accumulation

of volatile organic compounds near the ground, despite relatively high emission rates driven by slowly

decreasing temperature.

In an attempt to generalize the above-discussed ﬁndings, Figure 9 shows a simple conceptual

model, applicable to clear and calm days.

FFiigguurree 99.. CCoonncceeppttuuaall mmooddeell ooff bbiiooggeenniicc vvoollaattiillee oorrggaanniicc ccoommppoouunndd ((BBVVOOCC)) rreellaattiivvee ccoonncceennttrraattiioonn aatt

diﬀerent times during daylight hours, on clear and calm days. The horizontal bars in shades of gray

represent stable atmospheric layers. The curved lines in blue represent mixed layers. Curved lines in

green represent BVOC emissions from trees and soil, with lengths indicatives of the respective emission

rates. The east (E) and west (W) are indicated. Elements of the picture are not to scale.

Cloudiness prevents most of the solar radiation from reaching the ground and the tree foliage,

primarily leading to reduced BVOC emissions, as well as to the limitation of atmospheric vertical

mixing, with the latter hindering the ground accumulation of BVOCs early in the morning while

attenuating the vertical dilution around noon in comparison with clear conditions. Overall, based on

the results presented in Section 3, cloud cover seems to lead to lower BVOC concentrations near the

ground. Strong winds drive remarkable horizontal advection of substances in the atmosphere, which

can unpredictably lead to higher or lower BVOC local concentrations near the ground, depending on

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the presence, composition, and emission rates of forest stands on the windward side, as well as on other

uncontrollable factors such as turbulence, leeward wakes, and other disturbances to the atmospheric

vertical mixing.

Within the level of signiﬁcance allowed by the measurement campaigns carried out on a limited

sample of natural areas in central Italy, over a few days during less than three months between August

and October in a single year, and referring to the only daylight hours, some interpretation and a few

preliminary guidelines can be summarized as follows:

• Early in the morning, the soil heats up due to the emerging solar radiation, and a strong mixed

layer develops and grows in the atmosphere just above the ground, leading to a shallow unstable

boundary layer. Although BVOC emissions from trees are still limited by low levels of radiation

and temperature, BVOCs diﬀuse within a limited vertical layer and can accumulate near the

ground, up to relatively high concentration levels. Early morning could to be a relatively good

time for the contribution of BVOCs to forest healing eﬀects.

• Mid-morning, the atmospheric mixed layer grows rapidly in depth, driven by the increasing

radiation, while BVOC emissions are still moderate. As a result, BVOCs diﬀuse within a relatively

deep vertical layer and their accumulation near the ground can temporarily decrease in comparison

to early morning. Mid-morning could be a relatively disadvantaged time.

• In the hours just after noon, with solar radiation and air temperature around their peaks, BVOC

emissions peak too, leading to the highest concentrations near the ground despite the high dilution

rate of BVOCs within the deep atmospheric mixed layer. The middle of the day, and early

afternoon could be the best time for the contribution of BVOCs to forest healing eﬀects, provided

that other factors, such as those deﬁning the bioclimatic comfort, are at acceptable levels.

• Late in the afternoon, with vanishing solar radiation, a stable atmospheric layer develops just

above the ground, leading to a shallow stable layer with very limited vertical mixing, in turn

surmounted by a residual mixing layer. The combination of declining BVOC emissions, due to low

radiation levels and falling temperature, and the inhibition of their mixing from elevated sources

(tree foliage) down to the ground, can lead to the lowest concentration levels. Late afternoon

could be the most disadvantageous time for the contribution of BVOCs to forest healing eﬀects.

• With regard to BVOC inhalation, during clear and calm days, a preliminary planning suggestion

for hikers can be issued that forest trails should be preferably traveled in early morning and from

noon to early afternoon, rather than in mid-morning and late afternoon. Depending on hiking

miles, the latter periods could be used to rest at mountain refuges, or to walk through areas devoid

of forest vegetation.

• Cloudy or windy days appear less suitable at any time to enjoy the BVOC-related forest healing

eﬀects due to generally lower and largely unpredictable concentration levels, adding this ﬂaw to

the generally lower level of comfort.

• Based on the results of this study, and under the speciﬁc meteorological conditions, conifer trees

seemed to be more eﬃcient with regard to BVOC concentrations in the forest air, at least in

comparison with beech trees (the most widespread tree in Italy, concentrated in mountainous

areas and especially in the Apennines, particularly at elevations above 1200 m). Thus, when

diﬀerent alternatives are available, pure ﬁr or mixed beech-ﬁr forests could be preferred over pure

beech forests. However, the evidence was quite limited, and the above statement might not apply

to diﬀerent deciduous tree species, which are widespread at lower elevations.

The presented ﬁndings are partially contrasting with results recently obtained in Korea, where peak

BVOC concentrations were found around 17:00 pm, and the lowest in the early morning [36]. However,

diﬀerent sampling frequencies, forest environments and latitudes seriously limit the meaningfulness

of a comparison between the two studies. To the authors’ best knowledge, no other studies to date

match the requirements for a meaningful comparison.

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The advantages of using a PID for the measurement the concentrations of volatile organic

compounds in forest air consist of the very high measurement and logging frequency (2 s), allowing

to detect changes in real time on ﬁxed sites, and about every 2 m along paths. The portability of the

instrument, as well as the low cost of measurements represent further advantages. The results of this

study demonstrate that high frequency measurements are needed in order to capture the substantial

variability of BVOC concentrations in forest air, occurring within a few tents of minutes and several

hundred meters.

The main and substantial disadvantage consists of the unselective measurements, which leave

unknown the composition of the detected compounds and their safe attribution to plant emissions.

The detection of the speciﬁc composition of volatile organic compounds, enabling their attribution

to biogenic or anthropogenic sources and thus providing a more accurate representation of BVOC

concentration, with an analysis of possible changes in time and space of the composition of BVOCs in

the forest air, would require completely diﬀerent devices. For example, absorbent tubes that must be

deployed at least in triplicate at any point of measurement, require at least 60 min for any absorption

session, and must be thermally desorbed oﬄine [36].

The application of methods aimed at detecting the speciﬁc components of BVOCs, like the one

mentioned above, would be practically unfeasible in the case of paths and hiking trails. However,

a recommended direction for future research with respect to the characterization of forest sites and

paths in terms of BVOC concentrations concerns the coupling of a high-frequency PID with analytical

devices, such as absorbent tubes, in order to calibrate the PID-based measurements at selected sites.

This direction aims at deﬁning the relative contribution of biogenic compounds to the total

concentration of volatile organic compounds, and likely even more importantly the detailed composition

of BVOCs, which could change with season, time of day, weather conditions, composition of the forest,

and soil conditions [36]. Due to the remarkable specialization of diﬀerent components of BVOCs with

regard to their biological activities [39], the functionality, or healing eﬀectivity, of a forest site or path

would require the knowledge of the concentration not only of total BVOCs, but also of the relative

abundance of their most active constituents, and the respective variability in time and space.

Additional recommendations for further research can be summarized as follows:

• Beyond the quantities considered in this study, other meteorological disturbances such as drought

and accumulated rain in previous days should be taken into account.

• BVOC concentration daily cycles in diﬀerent seasons, such as spring, early summer, late autumn,

and winter, should be investigated, also aimed at building up comprehensive year-long models.

• Instead of data from sparse weather stations whose interpolation could lead to remarkable

uncertainties, the use of high-resolution, gridded meteorological data over the geographical

domain into consideration is recommended, for example extracted from reanalyses or very

short-term forecasts generated by high-resolution mesoscale atmospheric models.

• A substantial amount of research is needed in order to score diﬀerent tree types and forest

compositions with regard to their eﬀect on the variability of BVOC concentrations in the forest air,

including the dependence on season and weather conditions, as well as accounting for emissions

from both plants and soil.

This study should be considered as a starting point, and possibly as a methodological reference, for

further investigation and research, following the above-listed recommendations. However, the basic

ﬁnding and its consequences appear indisputable: as long as BVOCs are considered as an essential

resource contributing to forest healing eﬀects, detailed knowledge of the respective concentration

patterns in forest air and careful planning of practices are needed in order to substantially optimize the

beneﬁts for human mental and physiological health.

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5. Conclusions

Knowledge of the variability of BVOC concentrations in forest air could contribute to the

optimization of forest healing eﬀects. In particular, it could assist in planning forest therapy sessions

and practices, and allow hikers to beneﬁt more greatly from their walking along forest and mountain

trails. For the ﬁrst time, this study demonstrated that the variability scale of BVOC concentrations

could be comparable to the absolute concentration levels within time scales of less than one hour and

spatial scales of several hundred meters.

These results were achieved by using a photoionization detector that, while not allowing the

detection of individual components, allowed high-frequency measurements both on ﬁxed sites and

along paths. The remoteness of the study areas from anthropogenic sources, along with suitable data

processing, reasonably ensured the representativeness of the measurements of the total concentration

of volatile organic compounds with regard to the biogenic ones.

Based on empirical evidence, limited quantitative relationships, and a conceptual model,

provisional guidelines have been formulated about the evolution of BVOC concentrations during

daylight hours, suggesting the likelihood of peak BVOC concentration during few hours after noon, a

secondary peak in early morning, and lowest concentration in late afternoon during clear and calm

days. In addition, a very preliminary conclusion was drafted that conifer trees are more eﬃcient than

beeches with regard to BVOC concentration in forest air.

Author Contributions: Conceptualization, F.Z. and F.M.; methodology, F.M., F.Z., and L.A.; software, F.M., L.A.,

and G.B.; validation, F.M., L.A., and G.B.; formal analysis, F.M.; investigation, F.M. and L.A.; resources, F.M.; data

curation, L.A., G.B., and F.M.; writing—original draft preparation, F.Z. and F.M.; writing—review and editing,

F.Z., F.M., and G.B.; visualization, F.M. and L.A.; supervision, F.M. and F.Z.; project administration, F.Z. and F.M.;

funding acquisition, F.M. and F.Z.

Funding: Author F.M. received partial funding for this research from the Central Scientiﬁc Committee of the Italian

Alpine Club (CSC-CAI), project “The hidden treasure of conifers in the Tuscan-Emilian Apennines” (RiForest).

Acknowledgments: Massimo Albertazzi (Ion Science Italia S.r.l.) and Davide Comastri (Comastri Distribution

S.r.l.) are gratefully acknowledged for the granting of the Tiger VOC detector. Giuliano Cervi, Sonia Cuseri,

Giancarlo Tellini, Francesco Mantelli, Evelin Franceschini, and Marco Guiducci (Italian Alpine Club) are gratefully

acknowledged for very useful suggestions and invaluable logistic support during the measurement campaigns.

The authors are indebted to Francesco Becheri (“Pian dei Termini” farmer and psychotherapist, Italy) and Maurizio

Droli (University of Udine, Italy), who introduced the forest therapy and forest bathing concepts in Italy and

shared their brilliant ideas with us, as well as to Andrea Piotti (Institute of Biosciences and Bioresources, National

Research Council, Italy), who, with his team, is revolutionizing knowledge of the origin and real value of coniferous

forests in the Italian Apennines.

Conﬂicts of Interest: The authors declare no conﬂict of interest.

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