Determination of differences in temperature regimes on healthy and bark-beetle colonised spruce trees using a handheld thermal camera ...

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Determination of differences in temperature regimes on healthy and bark-beetle colonised spruce trees using a handheld thermal camera ...
iForest                                                                                                    Research Article
                                                                                                         doi: 10.3832/ifor3531-014
                                                                                                               vol. 14, pp. 203-211
         Biogeosciences and Forestry

Determination of differences in temperature regimes on healthy and
bark-beetle colonised spruce trees using a handheld thermal camera

Andrej Majdák (1),                               In this study, we compared the daily temperature regimes of healthy unin-
                                                 fected trees in the interior of a forest stand and at the fresh forest edge with
Rastislav Jakuš (1-2),                           infested trees at the forest edge in an area affected by a bark beetle out-
Miroslav Blaženec (1)                            break. We estimated the potential of a handheld thermal camera for early
                                                 identification of bark-beetle infested trees. We show that infested trees have
                                                 significantly higher trunk temperatures than uninfested trees, which is more
                                                 visible on the shine side of the trunk, and we report the differences in tem-
                                                 perature between the shine and shadow sides. The differences are more no-
                                                 ticeable on a warm, bright, and sunny day than on cold and cloudy day. The
                                                 different intensity of solar radiation does not affect the distinction between
                                                 infested and uninfested trees. The handheld thermal camera shows potential
                                                 for identifying bark-beetle infested trees by scanning tree trunks on bright
                                                 sunny days.

                                                 Keywords: Bark-beetle Infested Trees, Handheld Thermal Camera, Incoming
                                                 Solar Radiation, Norway Spruce, Solar Radiation Modelling, Temperature Dif-
                                                 ferences

Introduction                                    2013). Higher air temperatures at cleared         tion rates, and may eventually lead to trees
  Stands of mature Norway spruce (Picea         edges, associated with increased solar radi-      being subjected to drought stress (Kautz et
abies [L.] Karst.) are often attacked by Eu-    ation, predispose such edge trees to infes-       al. 2013, Marešová et al. 2020).
ropean spruce bark beetle (Ips typogra-         tation by providing favourable flight condi-        To some extent, trees can influence their
phus L.). In response to climatic changes       tions for bark beetles and by reducing host       thermal environment and thereby avoid
and especially to increases in maximal tem-     resistance mechanisms due to drought or           excessive heat or enhanced temperatures
peratures, the extent of damage caused by       thermal stress on dispersing beetles (Kautz       during otherwise hot conditions (Leuzinger
these beetles is significantly increasing       et al. 2013). Higher temperatures on sun-         & Körner 2007). According to Helliker &
(Mezei et al. 2017). In mountainous condi-      exposed bark can increase the emission of         Richter (2008), the morphological and
tions, I. typographus prefers to attack trees   primary bark beetle attractants (Baier &          physiological characteristics of a tree can-
on fresh forest edges or in small openings      Bader 1997, Hietz et al. 2005, Marešová et        opy work to maintain leaf temperatures
caused by wind damage, salvage cutting,         al. 2020). During host selection, bark bee-       near the optimal value for photosynthesis
or previous bark beetle infestation (Jakuš      tles prefer warmer trees (Kautz et al. 2013).     (about 21 °C), irrespective of tree species,
et al. 2011, Kautz et al. 2013). Undisturbed      Another factor is connected with sun-re-        latitude, or average growing season tem-
spruce stands are usually well protected        lated effects. A clear cut of a recent infesta-   peratures. In warmer climates, leaf temper-
against direct insolation by individual and/    tion patch will lead to sudden sun expo-          atures are lowered by evaporative cooling
or collective shading (Jakuš et al. 2011).      sure to large parts of the stems of the edge      and mechanisms that reduce the absorb-
Natural disturbances, such as windthrows        trees, which were previously located with-        ance of solar radiation, such as decreased
or bark beetle infestation gaps, create new     in a closed stand and are thus charac-            leaf angles. However, the architecture of
forest edges within a stand, which show a       terised by relatively short crowns. Sun ex-       an individual tree changes only marginally
sharp microclimatic gradient. The altered       posure without any prior adaptation to the        during a few weeks of drought. On bright,
microclimate is characterised by increased      altered microclimate, particularly on south-      warm days, the difference between canopy
solar radiation, wind exposure, higher tem-     facing cleared edges, may result in heat-         foliage and air temperature is mainly the
peratures, and lower humidity (Kautz et al.     damaged phloem and increased transpira-           result of transpiration. Longer drought pe-
                                                                                                  riods increase canopy foliage temperatures
                                                                                                  (Scherrer et al. 2011). Stress induced by an
   (1) Institute of Forest Ecology, Slovak Academy of Sciences, Ludovíta Štúra 2, 960 53 Zv-      invasion of insects or the onset of disease
olen (Slovak Republic); (2) Faculty of Forestry and Wood Sciences, Czech University of Life       leads to, among other symptoms, stomatal
Sciences, Kamýcká 1176, 165 21 Praha 6 - Suchdol (Czech Republic)                                 closure and, consequently, to increased
                                                                                                  leaf and canopy temperatures (Smigaj et
@ Andrej Majdák (andrej.majdak@gmail.com)                                                         al. 2015). This temperature rise can often
                                                                                                  be detected at the leaf level at an early
Received: May 21, 2020 - Accepted: Feb 23, 2021                                                   stage of infection by thermal imaging.
                                                                                                  However, research on the use of thermal
Citation: Majdák A, Jakuš R, Blaženec M (2021). Determination of differences in temperature       remote sensing approaches for tree health
regimes on healthy and bark-beetle colonised spruce trees using a handheld thermal camera.        monitoring has been limited (Smigaj et al.
iForest 14: 203-211. – doi: 10.3832/ifor3531-014 [online 2021-05-02]                              2015). The development of handheld ther-
                                                                                                  mal cameras has allowed thermal imaging
Communicated by: Carlotta Ferrara                                                                 to be extended to the diagnosis of the
                                                                                                  physiological status of both woodland

© SISEF https://iforest.sisef.org/                                   203                                                 iForest 14: 203-211
Majdák A et al. - iForest 14: 203-211

                                        trees and individual urban trees (Jones          have been so thoroughly girdled that mor-         Materials and methods
iForest – Biogeosciences and Forestry

                                        2004).                                           tality was assured long before any effects
                                          The cooling effect of sap flow can help        on sap velocity were observed.                    Research site
                                        keep tree bole temperatures lower. Ac-             Early detection of infested trees is crucial      The study plots were set up in a 90-year-
                                        cording to Hietz et al. (2005), during day-      for the effective management of bark bee-         old Norway spruce stand (Picea abies [L.]
                                        light hours, the bark is warmed by the sur-      tle outbreaks (Latifi et al. 2014). Infested      Karst.) on a moderately southwest-expos-
                                        rounding air and direct radiation. The high      trees begin to undergo changes in their           ed slope at 650-730 m a.s.l. in the Western
                                        water content of sapwood dampens the             spectral characteristics (Abdullah et al.         Carpathians, Central Slovakia, Michalová
                                        daily temperature fluctuations in the bole;      2018), which can be effectively detected us-      forest district (48° 45′ 55.85″ N, 19° 47′
                                        transpiration water passing through the          ing remote sensing (RS) techniques, e.g.,         31.18″ S; WGS84). The mean annual climate
                                        sapwood, which enters the stem base at           unmanned aerial vehicles (UAV), satellites,       indicators of the research site were as fol-
                                        the temperature of the soil, will remove         and thermal imaging (Lausch et al. 2016,          lows: air temperature, 4-6 °C; precipitation,
                                        heat and cool the cambium and the inner          Lausch et al. 2017). Thermal imaging, based       900-1000 mm; sum of global radiation,
                                        parts of the secondary phloem.                   on terrestrial sensors or handheld thermal        1100-1150 kWh m-2 (Lapin et al. 2002). The
                                          During attack and colonization, bark bee-      cameras, has been used for a wide range of        soil is classified as Dystric Cambisols and
                                        tles disrupt two basic life-sustaining trans-    conditions and with diverse plant species.        Cambic Umbrisols, associated with Lep-
                                        port processes of the trees they infest. In      The technique can be applied at different         tosols, from weathering products of acid
                                        the early phase of overcoming tree host          scales: from single seedlings/leaves (Buitra-     to neutral rocks (Lapin et al. 2002) accord-
                                        defences, adult beetles enter a suitable         go et al. 2016) to whole trees or field crops     ing to the World Reference Base (WRB)
                                        host by boring through the outer bark and        and regions (Costa et al. 2013). It shows sig-    classification system (IUSS Working Group
                                        into the phloem, and consume phloem tis-         nificant potential for studying plant-envi-       2014).
                                        sue to build egg galleries; developing lar-      ronment interactions and specific phenom-
                                        vae consume phloem for food until matu-          ena, such as stomatal closure, stress toler-      Research design and measurements
                                        rity. Together, phloem feeding by adults         ance, and the effects of different manage-          For our observations, three groups of
                                        and larvae contributes to some amount of         ment strategies on crop water status and          trees were selected. Two groups contained
                                        phloem girdling, disrupting the transport        tree health (Jones 2004, Reinert et al. 2012,     healthy trees, not infested by bark beetles,
                                        of photosynthate from the canopy to other        Costa et al. 2013). However, using a hand-        and one contained infested trees. There
                                        tissues within the tree (Paine et al. 1997,      held thermal camera for identifying bark-         were five trees in each group. The first
                                        Wullschleger et al. 2004, Hubbard et al.         beetle infested trees based on trunk tem-         group of healthy trees was selected in the
                                        2013). Later, phytopathogenic fungal             perature sensing has not yet been de-             forest interior (plot A, Interior_Uninfested)
                                        spores introduced by bark beetles germi-         scribed.                                          and the second at the newly created forest
                                        nate, and the spreading fungal hyphae              In our study, we aimed to compare daily         edge (plot B, Edge_Uninfested). The group
                                        penetrate the water-conducting xylem tis-        temperature regimes of healthy uninfested         of five infested trees (plot C, Edge_In-
                                        sue in the sapwood and block water trans-        trees in the stand interior and at a fresh        fested) was selected at another newly cre-
                                        port from the soil to the canopy (Wull-          forest edge and infested trees at the forest      ated forest edge close to the two groups
                                        schleger et al. 2004, Hubbard et al. 2013).      edge in areas affected by a bark beetle out-      of healthy trees, about 150 m apart. The
                                        Transpiration can begin to decline within        break. We also estimated the potential of a       trees were selected from the dominant
                                        the first weeks of beetle infestation. After     handheld thermal camera for early identifi-       and codominant trees in the forest stand,
                                        several weeks, pre-dawn water potential          cation of bark-beetle infested trees. We          and the mean values of selected tree char-
                                        drops significantly as water transport to        were specifically interested in the follow-       acteristics of the observed tree groups are
                                        the canopy significantly declines. In the        ing: (1) What is the proper height for sens-      listed in Tab. 1. The measurements were
                                        early stages, there may be no visible signs      ing trees for mutual comparison (base, 1.3        recorded in two days. The first day (20 Au-
                                        of needle discoloration (Kirisits & Offen-       m, 4 m, or crown) to find the differences         gust 2012) was sunny with high tempera-
                                        thaler 2002, Hubbard et al. 2013). The sub-      between uninfested and bark-beetle in-            tures, with a maximum air temperature in
                                        sequent death of the tree (staining or oc-       fested trees? (2) Is it possible to distinguish   the open area close to the forest edge
                                        clusion of sapwood, fading of foliage) may       between uninfested and bark-beetle in-            reaching 31.7 °C and the sum of global radi-
                                        occur long after the critical interactions be-   fested trees based on temperature? (3)            ation totalling 5588 Wm-2 (Fig. 1a). The sec-
                                        tween the tree and beetle/fungus complex         How much is the temperature difference            ond day (10 October 2012) was cloudy and
                                        (Paine et al. 1997). Wullschleger et al.         affected by direct solar radiation and does       cold, with a maximum air temperature of
                                        (2004) showed that when xylem function           that prevent the identification of infested       9.2 °C and sum of global radiation of 1452
                                        begins to fail, the progeny of attacking         trees? (4) Can phloem temperature be de-          Wm-2 (Fig. 1b). Twenty days before the first
                                        beetles would have already departed the          rived from thermal imaging by handheld            day of measurement, there was almost no
                                        tree, and the phloem and cambium would           thermal cameras?                                  precipitation; the total for this period was
                                                                                                                                           2.6 mm. This means that the conditions
                                                                                                                                           were not only hot but also relatively dry
                                                                                                                                           before the first day of measurement. The
                                         Tab. 1 - Mean values (± standard error, SE) of selected tree characteristics between
                                                                                                                                           weather characteristics in the 20 days be-
                                         the plots and results of ANOVA (F[1, 2], α = 0.05). (*): diameter at breast height; (**):
                                                                                                                                           fore each measurement day are presented
                                         trees creating the surrounding forest stand and assessed for the purpose of model-
                                                                                                                                           in more detail in Tab. 2.
                                         ling the light distribution in the MIXLIGHT model.
                                                                                                                                             Images of stem and crown temperatures
                                                                                                                                           were captured using a WH-8 thermal cam-
                                                                                DBH*               Height             Crown length         era (Wuhan Guide Infrared Co., Ltd.,
                                          Stats                 Plot
                                                                                (cm)               (m)                (m)
                                                                                                                                           China), with a focal plane array (FPA) and
                                          Mean tree             A               38.6 ± 1.80        37.2 ± 1.11        18.2 ± 0.92          uncooled microbolometer with a resolu-
                                          characteristics       B               34.0 ± 1.70        37.0 ± 1.08        16.7 ± 0.44          tion of 384 × 288 pixels. The spectral range
                                          (± SE)                                                                                           was 8-14 μm and the sensitivity was ≤ 0.08
                                                                C               36.0 ± 2.26        38.6 ± 0.93        17.6 ± 0.85
                                                                                                                                           °C at 30 °C. The emissivity of imaging was
                                                                other**         36.8 ± 0.49        38.7 ± 0.26        17.5 ± 0.27          set to 0.96. For trees in plot A (Interior_Un-
                                          ANOVA results         F[3, 103]         0.90               1.16              0.30                infested, two trees) and plot B (Edge_Un-
                                                                p-value           0.45               0.33              0.82
                                                                                                                                           infested, three trees), the temperature of
                                                                                                                                           phloem close to the place sensed by the in-

                                        204                                                                                                                        iForest 14: 203-211
Temperature differences on healthy and bark-beetle-colonised trees

                                                                                                                                            iForest – Biogeosciences and Forestry
     Fig. 1 - Daily course of
   global radiation and air
  temperature in an open
 area close to plots and in
 the forest interior during
   measurement days: (a)
 warm and sunny day and
  (b) cold and cloudy day.
    Air temperature in the
 open area is represented
   by a solid black line and
 by a solid grey line in the
     forest interior. Global
  radiation is represented
    by a dotted black line.

frared camera was recorded continuously         Tab. 2 - Course of weather characteristics in the 20 days before each day of measure-
using thermal sensors inserted into the         ment (20 August and 10 October 2012).
phloem (EMS, Brno, Czech Republic), con-
nected to a datalogger and stored in 15-
                                                 Parameter               Stats         31 July - 19 Aug. 2012    20 Sept. - 9 Oct. 2012
minute intervals. The obtained infrared pic-
tures were processed with IR Analyser            Air temperature         Avg                     17.6                    11.8
software (Wuhan Guide Infrared Co., Ltd.,        (°C)                    Min                      4.5                     -0.5
China). To eliminate local inaccuracies of                               Max                     34.2                    24.3
stem temperatures caused by sunlight pen-
etrating through the canopy, we selected         Relative air humidity   Avg                     72                      80
an area of about 20 × 20 cm of the ob-           (%)                     Min                     32                      37
served stem, from which the average tem-                                 Max                    100                     100
perature was obtained (Fig. 2).
                                                 Precipitation (mm)      Sum                      2.6                    30.6
  Thermal pictures of each tree trunk were
captured at three heights: at the base and       Global radiation        Avg                    4722                   2847
at 1.3 and 4 m on both the shine and             (W m-2 day-1)           Min                    1047                    786
shadow sides; the temperature of the tree
                                                                         Max                    6532                   5299
crown was taken from the ground. The
shine side was the part of the tree trunk
facing direct sun every time a thermal im-     shining on the plots. The last interval lasted    surements on all plots on the second day
age was captured, and the shadow side          two hours. We captured nine measure-              (10 October 2012). In the open area, air
was on the opposite side. The images were      ments on plots A (Interior_Uninfested) and        temperature and global radiation were
captured in approximately one hour inter-      B (Edge_Uninfested) and eight measure-            measured at half-hour intervals using a
vals from morning hours after sunrise to       ments on plot C (Edge_Infested) on the            Minikin RT® (EMS, Brno, Czech Republic).
evening hours when the sun was no longer       first day (20 August 2012), and nine mea-         Air temperature was simultaneously mea-

  Fig. 2 - Thermal image
    and RGB photo from
   1.3 m height captured
    using a thermal cam-
  era: (a) shine side of a
    tree; and (b) shadow
    side of a tree. On the
 thermal image, an area
  of approximately 20 ×
  20 cm in the middle of
 the observed stem was
  selected for obtaining
   the average tempera-
     ture. On the right or
  left side of the stem is
    an auxiliary scale visi-
 ble for easier identifica-
      tion of the required
  height on the thermal
                    image.

iForest 14: 203-211                                                                                                                   205
Majdák A et al. - iForest 14: 203-211
iForest – Biogeosciences and Forestry

                                         Fig. 3 - Vertical mean temperature profile from measurements on both shine and shaded sides of trees on (a) warm and sunny days
                                         and (b) cold and cloudy days. Mean temperatures from uninfested trees in the forest interior (plot A) are represented by dotted
                                         grey lines, from uninfested trees on the forest edge (plot B) by dashed grey lines, and from bark-beetle-infested trees on the forest
                                         edge (plot C) by solid grey lines. Solid black lines represent total mean temperatures from all plots. Statistically different groups of
                                         total mean temperatures between the heights on both shine and shaded sides of trees within each measuring day separately were
                                         determined according to Tukey’s test (α = 0.05) and are highlighted by different lowercase letters.

                                        sured in the forest interior using a Minikin exported individual solar radiation values      and plot B (Edge_Uninfested), where the
                                        TH® (EMS, Brno, Czech Republic).              at the selected height and for a particular    phloem temperature was measured, were
                                                                                      measurement time for each tree measured        used in the analysis.
                                        Solar radiation modelling                     by the thermographic camera.
                                          The amount of solar radiation at each                                                      Results
                                        measurement point (height on the stem) Statistics
                                        was recalculated using the MIXLIGHT mod-        The data were tested by Levene’s homo-       Vertical temperature profile and
                                        el (Stadt & Lieffers 2000), which is used to geneity test and the Shapiro-Wilk normality     optimal height for thermal
                                        calculate solar radiation passing through test. Given the test results, the data met         measurement
                                        tree crowns. The input to the model was the assumptions for parametric statistical             The total mean temperature of the stem
                                        data obtained with an Ilris HD ® terrestrial methods and were statistically evaluated in     base on a warm and sunny day on the
                                        laser scanner (Teledyne Optech, Canada). R.                                                  shine side in all plots was the highest (Fig.
                                        The scanning method was chosen to pro-          (1) To determine the appropriate height      3a) and significantly different (F = 141.9, df
                                        duce the best possible representation of for thermal camera measurements, we                 = 7, p < 0.001) from temperatures at other
                                        the forest stand structure. The focus was used repeated-measure ANOVA (a = 0.05)             heights. With increasing measurement
                                        not only on selected trees in individual for testing the temperatures at each tree           height, temperatures decreased, whereas
                                        plots, but on all trees at a distance of at height: at the base, at 1.3 and 4 m, and at      at heights of 1.3 and 4 m did not show sta-
                                        least 3 times the average height of trees the crown, separately for the two mea-             tistically significant differences among
                                        from experimental areas. The point cloud surement days. The relevance of the tree            groups but differed from crown tempera-
                                        was processed in the Polyworks™ v. 12 soft- to the individual plot (plot A, Interior_Unin-   ture. Temperatures on the shady side were
                                        ware environment (InnovMetric Software, fested; plot B, Edge_Uninfested; and plot            balanced along the full height profile; to-
                                        Canada), where the scan was then georef- C, Edge_Infested) and the sensing time              gether with the crown temperature on
                                        erenced into the WGS84 geodetic system. was not considered. Tukey’s test was used            shine side, they did not show statistically
                                        Geometric characteristics of the trees were to determine statistically different groups.     significant differences among groups. On
                                        obtained manually from the created point        (2) To identify the temperature differ-      the cold and cloudy day (Fig. 3b), the mean
                                        cloud. The parameters that were detected ences in 1.3 m height between trees on              temperatures also decreased with mea-
                                        were tree height, diameter at breast height each of the three plots based on individual      surement height on both sides of the trees.
                                        (DBH), trunk coordinates, crown deploy- time of measurement and sunny and shady              The highest mean temperature was ob-
                                        ment height, crown parameters, and tree sides, we used ANOVA (α = 0.05) followed             served at the stem base from the shine
                                        social status. After entering the tree char- by Tukey’s test.                                side and did not differ significantly from
                                        acteristics and other characteristics, such     (3) To determine the role of incoming so-    temperatures at heights of 1.3 and 4 m, but
                                        as slope, orientation, geographic position lar radiation on the temperature of the           differed from crown temperature (F =
                                        of the area, and time (or time interval), the trees in each individual plot, we used out-    28.51, df = 7, p < 0.001). The mean stem
                                        model quantifies the percentage of solar puts from the MIXLIGHT model containing             temperatures on the shady side together
                                        radiation passing through the forest stand. information on the recalculated global radi-     with crown temperatures on both sides did
                                        We used mean values from 10 minute inter- ation for individual trees and the individual      not show statistically significant differ-
                                        vals of solar radiation at the time of ther- measuring times as covariates in the AN-        ences among groups.
                                        mographic camera measurement. Using COVA test (α = 0.05).
                                        real solar radiation data from the weather      (4) To determine the dependence of tree      Differences between healthy and bark-
                                        station converted with MIXLIGHT data, we surface temperature and phloem tempera-             beetle infested trees
                                        were able to calculate the real amount of ture, we used linear correlation analysis.          The temperature course on the warm and
                                        solar radiation. Using a Python script, we Trees from plot A (Interior_Uninfested)           sunny day (Fig. 4a) shows that bark-beetle

                                        206                                                                                                                  iForest 14: 203-211
Temperature differences on healthy and bark-beetle-colonised trees

                                                                                                                                            iForest – Biogeosciences and Forestry
   Fig. 4 - Mean temperature ± standard error
       (SE) at 1.3 m above the ground from the
 shine and shaded sides of trees and temper-
      ature difference ± SE between both sides
   separately for both days of measurements:
      (a) warm and sunny; (b) cold and cloudy.
         Statistical differences in temperatures
 between plots according to Tukey’s test (α =
    0.05) at particular measurement times are
     separately highlighted by different lower-
   case letters at the top of subgraphs. The X-
    axis is divided for each plot (A, B, C) within
        each measurement, indicated by corre-
    sponding measurement times. Uninfested
 trees in the forest interior (plot A) are repre-
  sented by solid black lines, uninfested trees
       on the forest edge (plot B) by solid grey
   lines, and bark-beetle infested trees on the
     forest edge (plot C) by dotted black lines.

infested trees (plot C) had statistically sig- ments than the uninfested trees on the for- edge (plot B) and interior (plot A) trees, re-
nificantly higher temperatures on the shine est edge (plot B). The temperatures of un- mained similar for the first four measure-
side since the first measurement than the infested trees from the shine side, both ments. They began to differ significantly
uninfested trees on the forest edge (plot
B) and in the forest interior (plot A). The
temperature remained above 50 °C for
most of the day, with first and last mea-
surements being above 40 °C, which dif-
fered from the uninfested trees in the for-
est interior, whose temperatures did not
exceed 33 °C. The temperatures from the
first six measurements were significantly
higher compared to those of uninfested
trees on both the shine and shaded sides.
The temperatures of uninfested trees,
both edge and interior, were similar for the
first two measurements, with minimal dif-
ferences between shine and shaded sides.
The temperatures of uninfested trees on
the forest edge and the interior began to       Fig. 5 - Mean crown temperature ± SE from the shine side of trees for both measure -
differ from the third measurement on the        ment days: (a) warm and sunny; (b) cold and cloudy. Statistical differences in temper -
sunny side and the fourth on the shadow         ature between plots according to Tukey’s test (α = 0.05) at particular measurement
side.                                           times are separately highlighted by different lowercase letters at the top of sub-
  The temperature course on the cold and        graphs. The X-axis is divided for each plot (A, B, C) within each measurement, indi-
cloudy day in Fig. 4b shows that bark-bee-      cated by corresponding measurement times. Uninfested trees in the forest interior
tle infested trees (plot C) had statistically   (plot A) are represented by solid black lines, uninfested trees on the forest edge (plot
significant higher temperatures on the          B) by solid grey lines, and bark-beetle-infested trees on the forest edge (plot C) by
shine side during the first three measure-      dotted black lines.

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Majdák A et al. - iForest 14: 203-211

                                                                                                                                                                                     from the fifth measurement. The tempera-
iForest – Biogeosciences and Forestry

                                         Tab. 3 - Results of ANCOVA comparison (F, df, p) at α = 0.05 between plots for shine                                                        ture courses of both sides of uninfested
                                         and shadow sides of trees and different measurement days.                                                                                   trees in the interior were similar, with the
                                                                                                                                                                                     difference not exceeding 1 °C. The results
                                                                                                                                                             ANCOVA results
                                              Day Side Plot comparisons                                                                                                              from the cold and cloudy day showed that
                                                                                                                                                      df        F      p-value       the infested trees also had significantly
                                                                                                      Interior_Uninfested (A) - Edge_Uninfested (B)   1        1.02       0.316      higher temperatures on the shine side
                                                                                   Shine
                                              warm and sunny

                                                                                                      Interior_Uninfested (A) - Edge_Infested (C)     1       49.77
Temperature differences on healthy and bark-beetle-colonised trees

Relationship between tree stem surface           distance). Based on our results, we deter-      trees on the forest edge (plot B) and in the

                                                                                                                                                  iForest – Biogeosciences and Forestry
temperature and phloem temperature               mined the optimal height of this measure-       forest interior (plot A), we report a strong
  A significant coefficient of determination     ment to be 1.3 m. An important factor is        correlation between phloem and bark sur-
(R2 = 0.92) for the shine side with a mean       the angle of measurement, which should          face temperatures. This agrees with the re-
temperature of 22.9 °C from the thermal          be perpendicular to the measured surface,       sults reported by Powell (1967) and Hietz
camera and 18.5 °C from thermal needles          as recommended by the manufacturer, to          et al. (2005), and also demonstrates the
was obtained (Fig. 6a). The most sun-ex-         achieve the highest accuracy. However, we       precision of thermal camera measurement,
posed were the uninfested trees on the           recorded almost equal temperatures on           which has potential for tree physiology and
forest edge (plot B) with the mean surface       the tree trunk 1.3 m above the ground on        bark beetle development modelling. The
temperature of 40.5 ± 2.54 °C (Tab. 4) and       the shine side. This indicated that for other   most extreme values of surface bark tem-
mean phloem temperature of 34.4 ± 1.61 °C.       thermal camera applications, the whole          peratures on uninfested trees were re-
However, starting with the fourth mea-           profile of the tree trunk can be used. For      corded on the forest edge (plot B) from
surement, the surface temperatures were          example, scanning forest edges from             the shine side during the warm and sunny
above 40 °C with a maximum of 54.4 °C and        greater distances would be possible, focus-     day, especially during noon and afternoon.
a mean of 48.6 °C. In contrast, phloem tem-      ing on the part of the tree between the         During this period a maximum of 54.4 °C
peratures were above 33 °C with a maxi-          trunk base and the crown deployment             was recorded on the bark surface, but the
mum of 43.5 °C and a mean of 39 °C. The          height.                                         temperatures recorded in the phloem were
mean difference between the stem surface           On the shaded side, the soil surface has a    on average 9.6 °C lower. This agrees with
and the phloem temperatures during this          stronger influence, heating the tree stems.     the study of Nicolai (1986), who described
period was 9.6 °C. For the shadow side, a        The temperature is highest at the base and      the insulating properties of bark in differ-
significant coefficient of determination (R 2    gradually decreases upward along the            ent tree species and types of bark. Accord-
= 0.92) with a mean temperature of 17.72 °C      stem. On the shine side, the temperature is     ing to Annila (1969), not only temperature
from the thermal camera and 15.34 °C from        more directly determined by direct solar ra-    but also relative humidity affects the sur-
thermal needles was obtained (Fig. 6b).          diation.                                        vival of adults and offspring of Ips typog-
                                                                                                 raphus. The relative humidity is naturally
Discussion                                       Differences between trees in forest             higher in the galleries under the bark and
                                                 stand interior and at newly created             thus reduces the risk of mortality from dry-
Vertical temperature distribution                forest edge                                     ing out. Larvae, as well as pupae and
  Our results showed that the temperature          Healthy or infested trees on forest edges     adults, survived at 45° and 46 °C for 6
on the trunk base is influenced not only by      had higher temperatures than trees in the       hours, at 47 °C for 4 hours and at 48 °C for 2
solar radiation, but also by the local micro-    stand interior. This corresponds with the       hours. Only temperatures exceeding 47 °C
climate. A strong effect is related to dis-      preference of I. typographus to attack trees    appear to be fatal in the wild, but such
tance from the soil surface. The tempera-        on forest edges (Jakuš et al. 2011, Kautz et    temperatures only stay for a few hours and
ture at the trunk base is much higher com-       al. 2013). A higher level of solar radiation    the bark beetles survive this without loss.
pared to other measurement heights. Tem-         generally increases surface temperature.        Karasev et al. (2017) used semiconductor
peratures are higher on the sunny part of        Due to the effect of transpiration, the sur-    thermoresistors to detect trends in stem
the trunk. This agrees with our observa-         face temperature of relatively healthy          temperatures of Scots pine in different
tions of early spring bark beetle attacks on     trees on the forest edge did not increase       groups based on the physiological state of
forest edges in NP Šumava (Jakuš R, un-          directly with exposed irradiation, as ob-       trees. The temperature was found to have
published observations). In spring swarm-        served for the infested ones. Our results       a strong inverse correlation with the state
ing, bark beetles first attack trees on forest   correspond with those of Hietz et al.           of the trees, confirming that the method of
edges at the base of the trunk (Zumr 1985).      (2005), especially with the described cool-     assessing physiological state using temper-
Contrary to our findings, Powell (1967) re-      ing effect of transpiration on sapwood and      ature parameters allows early diagnosis of
ported lower temperatures at the base of         cambium temperature.                            decreased viability of conifers.
lodgepole pine trunks than the rest of the         With lower irradiation, healthy trees on
bole. Although it is a different species from    the forest edge maintained their surface        Canopy layer
Norway spruce, both species have similarly       temperatures near those of trees in the in-       Only a few studies have focused on bark
finely scaly bark with similar thermal prop-     terior. In the case of interior trees, we       beetle detection using UAVs (Senf et al.
erties (Nicolai 1986). So, according to Pow-     found a similar temperature pattern for         2017, Hall et al. 2016). For example, Näsi et
ell (1967), possible contributing factors to     shine and shaded parts of the trunk. This is    al. (2015) and Näsi et al. (2018) distin-
the lower temperatures at the base in-           caused by low irradiation in the stand inte-    guished between healthy and infested and
cluded the lower temperature of xylem wa-        rior and the forest stand microclimate.         dead trees with overall accuracies of 76%
ter coming from the roots, conduction of                                                         and 81%, respectively, using hyperspectral
heat between the trees and ground, in-           Differences between healthy and bark-           UAV-borne images in Finland; however,
creased bark thickness nearer to the             beetle infested trees                           they did not distinguish between healthy
ground, and lower air temperature near             Bark-beetle infested trees on the forest      trees and those in an early stage of infesta-
the ground that persisted for most of the        edge had higher trunk temperatures than         tion.
24 h period within the forest stand. It          healthy trees on the forest edge and in the       Using a handheld thermal camera, we
seems that the base of the trunk is strongly     interior, whereas both groups of trees on       measured the bottom, and shady part of
influenced by many factors that affect the       the forest edge were exposed to similar         the crown, and our study is thus limited.
microclimate of the tree. Powell (1967) in-      amounts of incoming solar radiation. This       Measuring crown temperature from the
dicated higher trunk sections as being           agrees with the results of Powell (1967) on     bottom is not the most appropriate
more similar in temperature. We concluded        lodgepole pines infested by Dendroctonus        method. We cannot be sure of the temper-
that the temperature at the trunk base was       ponderosae. According to that study, fresh-     atures on the sunny/upper part of the can-
not appropriate for further analysis.            ly infested trees had subcortical tempera-      opy because significant temperature differ-
  Crowns tend to maintain stable tempera-        tures similar to those of uninfested ones.      ences could exist between the upper and
tures, even on infested trees. The measure-      However, as the beetle broods developed,        lower parts of the crown (Reinert et al.
ments of crown temperatures were not             the water content of the sapwood low-           2012).
suitable for further analysis of these differ-   ered, and the brood experienced higher            We can assume that the healthy canopy
ences because this would involve different       subcortical temperatures and greater ex-        layer of uninfested trees tends to cool by
types of measurement (i.e., surface and          tremes of temperature. On uninfested            transpiration and maintains stable and ho-

iForest 14: 203-211                                                                                                                        209
Majdák A et al. - iForest 14: 203-211

                                        mogeneous temperatures (Helliker & Rich-           tic-information systems for improving the IUSS Working Group WRB (2014). World refer-
iForest – Biogeosciences and Forestry

                                        ter 2008). Air flow could also be an impor-        efficiency of management”, supported by ence base for soil resources 2014. World Soil
                                        tant factor regulating the temperature of          the Research & Development Operational Resources Reports no. 106, FAO, Rome, Italy,
                                        the crown layer. Even the canopies of bark-        Programme funded by the ERDF; (3) Grant pp. 192.
                                        beetle infested trees had temperatures             Agency of the Ministry of Education and Jakuš R, Edwards-Jonášová M, Cudlín P, Blaenec
                                        similar to healthy trees. This may be due to       the Slovak Academy of Sciences (VEGA M, Jeík M, Havlíček F, Moravec I (2011). Charac-
                                        bark beetles attacking phloem (Wermelin-           2/0176/17); (4) EXTEMIT-K grant no. Z.02.1. teristics of Norway spruce trees (Picea abies)
                                        ger 2004). Sap flow and cooling by transpi-        01/0.0/0.0/15_003/0000433, financed by surviving a spruce bark beetle (Ips typographus
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