Pollen production of downy birch (Betula pubescens Ehrh.) along an altitudinal gradient in the European Alps

Abstract

High-altitude environments are highly susceptible to the effects of climate change. Thus, it is crucial to examine and understand the behaviour of specific plant traits along altitudinal gradients, which offer a real-life laboratory for analysing future impacts of climate change. The available information on how pollen production varies at different altitudes in mountainous areas is limited. In this study, we investigated pollen production of 17 birch (Betula pubescens Ehrh.) individuals along an altitudinal gradient in the European Alps. We sampled catkins at nine locations in the years 2020-2021 and monitored air temperatures. We investigated how birch pollen, flowers and inflorescences are produced in relation to thermal factors at various elevations. We found that mean pollen production of Betula pubescens Ehrh. varied between 0.4 and 8.3 million pollen grains per catkin. We did not observe any significant relationships between the studied reproductive metrics and altitude. However, minimum temperature of the previous summer was found to be significantly correlated to pollen (rs = 0.504, p = 0.039), flower (rs = 0.613, p = 0.009) and catkin (rs = 0.642, p = 0.005) production per volume unit of crown. Therefore, we suggest that temperature variability even at such small scales is very important for studying the response related to pollen production.

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International Journal of Biometeorology
https://doi.org/10.1007/s00484-023-02483-7
ORIGINAL PAPER
Pollen production ofdowny birch (Betula pubescens Ehrh.)
alonganaltitudinal gradient intheEuropean Alps
SurendraRanpal1 · SusannevonBargen2 · StefanieGilles3 · DariaLuschkova3 · MariaLandgraf2·
ClaudiaTraidl‑Homann3 · CarmenBüttner2 · AthanasiosDamialis3,4 · SusanneJochner‑Oette1
Received: 2 March 2023 / Revised: 24 April 2023 / Accepted: 24 April 2023
© The Author(s) 2023
Abstract
High-altitude environments are highly susceptible to the effects of climate change. Thus, it is crucial to examine and understand
the behaviour of specific plant traits along altitudinal gradients, which offer a real-life laboratory for analysing future impacts
of climate change. The available information on how pollen production varies at different altitudes in mountainous areas is
limited. In this study, we investigated pollen production of 17 birch (Betula pubescens Ehrh.) individuals along an altitudinal
gradient in the European Alps. We sampled catkins at nine locations in the years 2020–2021 and monitored air temperatures.
We investigated how birch pollen, flowers and inflorescences are produced in relation to thermal factors at various elevations.
We found that mean pollen production of Betula pubescens Ehrh. varied between 0.4 and 8.3 million pollen grains per catkin.
We did not observe any significant relationships between the studied reproductive metrics and altitude. However, minimum
temperature of theprevious summer was found to be significantly correlated to pollen (rs = 0.504, p = 0.039), flower (rs = 0.613,
p = 0.009) and catkin (rs = 0.642, p = 0.005) production per volume unit of crown. Therefore, we suggest that temperature
variability even at such small scales is very important for studying the response related to pollen production.
Keywords Plant ecology· Elevation· Mountain-valley gradient· Thermal factors· Reproduction· Air temperature
Introduction
Plant traits such as phenology and tree growth have
been repeatedly reported to be very sensitive to ongoing
climate change (Dobbertin 2005; Menzel etal. 2006,
2020). For plant species, this sensitivity is amplified at
Athanasios Damialis and Susanne Jochner-Oette equally
contributed.
* Surendra Ranpal
surendra.ranpal@ku.de
Susanne von Bargen
susanne.von.bargen@agrar.hu-berlin.de
Stefanie Gilles
stefanie.gilles@tum.de
Daria Luschkova
Daria.luschkova@tum.de
Maria Landgraf
maria.landgraf@agrar.hu-berlin.de
Claudia Traidl-Hoffmann
claudia.traidl-hoffmann@tum.de
Carmen Büttner
carmen.buettner@agrar.hu-berlin.de
Athanasios Damialis
dthanos@bio.auth.gr
Susanne Jochner-Oette
susanne.jochner@ku.de
1 Physical Geography/Landscape Ecology andSustainable
Ecosystem Development, Catholic University ofEichstätt-
Ingolstadt, 85072Eichstätt, Germany
2 Albrecht Daniel Thaer-Institute forCrop andAnimal
Sciences, Division Phytomedicine, Humboldt-University
ofBerlin, Berlin, Germany
3 Environmental Medicine, Faculty ofMedicine, University
ofAugsburg, Augsburg, Germany
4 Terrestrial Ecology andClimate Change, Department
ofEcology, School ofBiology, Faculty ofSciences, Aristotle
University ofThessaloniki, 54124Thessaloniki, Greece

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the limits of species distribution (Mellert etal. 2016),
where the ecological conditions do not meet the optimal
requirements for plant survival and growth. Cold-
adapted plant species growing at higher elevations in the
European Alps are especially susceptible to the effects of
climate change (Albrich etal. 2020; Engler etal. 2011),
and tree species at the tree line were reported to be more
sensitive to environmental changes (Wielgolaski etal.
2017). In general, mountain ecosystems allow studying
climate change impacts as they cover a variety of changes
related to abiotic and biotic factors along the elevational
gradient (Tito etal. 2020). For instance, air temperature
decreases by on average 0.5°C for every 100m of
elevation, as reported for the Bavarian Alps, Germany
(Kirchner etal. 2013). Studying plant responses using
such lapse rates can be easily translated into thermal
responses as often applied in phenological research
(Cerlini etal. 2022; Damialis etal. 2020; Jochner etal.
2012). The plants’ behavior along an altitudinal gradient
provides indications on potential impacts of climate
change at small horizontal distances (Damialis etal.
2011; Jochner etal. 2012).
It is already widely documented that the flowering time
of many spring flowering species has shifted earlier in the
year due to increases in temperature (Khanduri etal. 2008;
Menzel etal. 2020; Ziello etal. 2009). In addition to this
well-known response in phenology, pollen production of dif-
ferent species was found to be affected by factors related to
global change (Ladeau and Clark 2006; Ziska etal. 2003).
However, most of these studies refer to warming experi-
ments, and only very few studies assessed climate change
impacts in real-life ecosystems, either in urban or rural and
mountainous environments (e.g. Charalampopoulos etal.
2013; Damialis etal. 2011, 2020; Jochner etal. 2012).
Knowledge of changes in pollen production is important
for inter alia predicting crop yield in agriculture (González-
Fernández etal. 2020) and seed production in forestry
(Allison 1990). Furthermore, exposure to airborne
pollen of certain plant taxa provoke immune responses
and allergic symptoms in sensitized individuals (Buters
etal. 2012; D’Amato etal. 2007; Damialis etal. 2019).
Even though there are sophisticated European models
of airborne pollen abundance and timing (e.g. SILAM,
Sofiev etal. 2015) including inter-seasonal variations of
the potential amount of pollen emission (Verstraeten etal.
2019), most of them have not incorporated information on
pollen production, which undoubtedly plays a vital role in
forecasting the intensity of the airborne pollen season and
associated allergic symptoms. Information on individual-
specific values of pollen production can help understand
the involved processes that contribute to modifications of
pollen concentrations and hence might be important for
implementation in pollen forecasting systems.
The assessment of pollen production and the extraction
methods are not standardized, and most previous studies
were descriptive in nature reporting quantitative estimates of
single species and/or single locations (Fernández-González
etal. 2020; Hidalgo etal. 1999; Khanduri and Sharma 2009;
Molina etal. 1996; Subba Reddi and Reddi 1986). The spa-
tial extent is larger (horizontally or vertically) when examin-
ing the influence of urbanization or altitude as these studies
are based on environmental gradients (Damialis etal. 2011;
Fotiou etal. 2011; Jochner etal. 2011; Ziska etal. 2003).
However, there is still limited research on flower and/or pol-
len production along elevation gradients. This understanding
is important since it would give information on the plant’s
plasticity and how different environmental conditions impact
reproductive traits (Charalampopoulos etal. 2013). Few
studies assessed and attempted to explain pollen production
of several woody species along elevation gradients, namely
Corylus avellana, Cupressus sempervirens, Olea europaea,
Pinus halepensis, Platanus orientalis and Quercus coccifera,
mostly in Mediterranean regions (Aguilera and Valenzuela
2012; Charalampopoulos etal. 2013; Damialis etal. 2011;
Rojo etal. 2015), and Alnus incana in the Nordic region
(Moe 1998). Reproduction studies conducted along altitu-
dinal gradients mainly focus on characteristics of seeds, e.g.
seed quality, germination rate or weight (Allen etal. 2012;
2014). For birch species, Holm (1994) studied the repro-
ductive patterns along an altitudinal gradient in Northern
Sweden. So far and to the best of our knowledge, no previous
study has investigated the variation of pollen production of
birch at different altitudes. There has been a general lack of
studies examining the pollen production of anemophilous
species within alpine ecosystems as well as in the European
Alps. In contrast, there are some studies on differences in
birch pollen concentration in ambient air along altitudinal
gradients in the Alps (Gehrig and Peeters 2000; Jochner
etal. 2012; Wörl etal. 2022) and on pollen abundance and
its correlation with allergic symptoms and immune reactions
in sensitised patients (Damialis etal. 2019).
Birch (Betula spp.) trees are widely distributed across
the Northern Hemisphere (Atkinson 1992), and their pol-
len are highly allergenic (D’Amato etal. 2017) and present
a major cause of allergic rhinitis in central and northern
Europe (Biedermann etal. 2019). They often grow in low-
lands, although they are also present at higher altitudes
(Emberlin etal. 2002). In Germany, birch is found up to
an altitude of approx. 1800m a.s.l. (DWD 1991). The lat-
est citizen-science generated data demonstrated that Betula
pubescens (downy birch) can occur at altitudes as high as
1840m a.s.l., and Betula pendula (silver birch) was found
at a maximum altitude of 1610m a.s.l. in the Bavarian
Alps (BAYSICS Webportal). Based on future projections
using IPCC scenarios, birch trees in Bavaria are anticipated
to become less common at lower elevations but shift their

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treeline and become more dominant at higher elevations in
the Bavarian Alps over the next half century (Rojo etal.
2021). Spatiotemporal studies on birch pollen concentrations
in the Bavarian Alps have also shown the effect of differing
meteorological conditions such as wind patterns on birch
pollen concentration (Jochner etal. 2012). Therefore, the
estimation of actual and prospective pollen production and
knowledge on spatial and temporal variations are important
for forecasting future effects on respiratory allergies.
In the current work, we studied pollen production of
Betula pubescens along a valley-mountain gradient in the
Bavarian Alps for 2 consecutive years (2020 and 2021). The
main aim of this work was to quantify the production of
birch pollen, flowers and inflorescences (i.e. catkins) at sites
ranging from 700 to 1220m a.s.l. In addition, the relation-
ship between reproductive metrics and thermal parameters
was studied.
Materials andmethods
Study area
The study area was located in southern Bavaria (Germany)
and Tyrol (Austria) in the topographically complex region of
the Zugspitze area (Fig.1). With 2962m a.s.l., the Zugspitze,
which belongs to the Northern Limestone Alps in the Wetter-
stein Mountains, presents the highest mountain in Germany
(Jochner etal. 2012). The birch trees were located in the
city of Garmisch-Partenkirchen (700m a.s.l.) and followed
an altitudinal gradient up to the lake Eibsee (1000m a.s.l.)
and Ehrwald in Austria (1100m a.s.l.). The highest location
was at 1220m a.s.l. (Ehrwald Cable Car Station); thus, the
study covers an elevational gradient of 522m. At lower sites,
meadows are dominating; at higher elevations until approx.
1800m, forests with spruce as the dominating tree species.
The average annual temperature recorded at Garmisch-
Partenkirchen is 7.7°C and the average precipitation
sum amounts to 1373mm (1991–2020). For the years
2019–2021, the average temperature and total precipita-
tion at Garmisch-Partenkirchen are 7.9°C and 1315mm
(in 2019), 6.1°C and 1419mm (in 2020), and 7.4°C and
1434mm (in 2021), respectively (Fig.2) (DWD 2022).
Birch tree selection andinflorescence sampling
For assessing pollen production, we studied the species Bet-
ula pubescens Ehrh. The selection of individual trees was
based on their presence, and the criteria of accessibility of
the site and the reachability of catkins. Consideration was
given to have at least one site for every 100m of differ-
ence in elevation and to have representatives especially at
the lowest (700–900m; nine individuals) and highest sites
(> 1100m; six individuals) (Table1). We collected inflores-
cence samples from 17 trees at nine locations (Table1) in
spring 2020 and 2021.
Fig. 1 Location of the study sites in Germany/Austria (Eurostat GISCO) and in the Zugspitze region (NASA JPL 2020). Red dots: nine birch
tree locations (with in total 17 birch individuals). White font locations are in Germany and black font locations are in Austria

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After catkin elongation was initiated and before
anthesis, male catkins with mature and closed anthers
were collected in March and April 2020 and 2021. Cat-
kins were harvested in all four cardinal directions from
various branches at reachable heights (1.5 to 2m a.g.l.).
We also assessed tree parameters that were used for the
extrapolation of pollen production from catkins to the
crown volume: the height of the crown using Suunto PM-
5/1520PC Height Meter and the crown diameter, which
was computed by averaging the crown’s two widest per-
pendicular diameters. We counted the number of catkins
inside a sampling cuboid in the crown with a volume of
50cm × 50cm × 50cm and selected those areas of the
tree crown that represent the typical distribution of catkins
(Damialis etal. 2011).
Pollen extraction method
We adapted the method of Damialis etal. (2011) for the
extraction of birch pollen grains from closed inflores-
cences. The length and width (at the broadest point) of
one medium-sized inflorescence from each cardinal direc-
tion and per tree were measured, and the number of flow-
ers was counted. Then, each catkin was immersed in a
10% KOH solution overnight (Faegri etal. 1989; Moore
etal. 1991; Ranpal etal. 2022). After boiling the solu-
tion the next day at 120°C for 10min, the soft catkin was
mashed with a glass rod to discharge pollen. We added
a bipolar solvent, glycerol (70%), to a volume of 20mL
(Ranpal etal. 2022) to prevent pollen from clustering
(Shivanna and Rangaswamy 1992); safranin was applied
as a stain. Using a VITLAB® micropipette, two aliquot
samples (10 µL each) of each suspension were taken
while the mixture was continuously stirred to achieve
homogeneity. The extraction was then placed on micro-
scope slides and covered with slips. We then counted the
pollen grains on these slides using a 100 × magnification
(Zeiss AXIO Lab.A1, Germany). In case of a substantial
difference in the pollen counts between these two slides
(> 30%), the progress was repeated to increase homogene-
ity of the suspension.
We estimated pollen production for different scales fol-
lowing the formulae mentioned by Damialis etal. (2011).
The number of pollen grains per catkin (Pca) was calculated
by multiplying the number of pollen grains on a microscope
slide with the ratio of the volumes of the suspension (20mL)
and the sample taken (10 µL). Following, the number of
pollen grains per flower (
Pfl
) was derived as a quotient of
Fig. 2 Monthly meteorological data recorded at DWD station
Garmisch-Partenkirchen for the years 2019–2021. Solid lines show
monthly average temperature: 2019 (orange), 2020 (dark blue) and
2021 (red) and blue bars the monthly precipitation sum: 2019 (dark
blue), 2020 (blue) and 2021 (light blue). x-axis: months, left y-axis:
monthly mean temperature in °C, right y-axis: monthly precipitation
sum in millimetres. Mean values (1991–2020) are displayed as black
dashed line (temperature) and grey bars (precipitation sum). Data:
DWD 2022
Table 1 Description of the location of the trees selected for studying
their pollen production, including their coordinates, mean altitude
(m a.s.l.) and number of the trees at each site in the Garmisch-
Partenkirchen area
Location Coordinates Altitude
(m a.s.l.) n trees
Kurpark N 47°29′46″E 11°05′26″696 1
Hindenburg N 47°29′47″E 11°06′19″706 1
Alpspitzbahn N 47°28′18″E 11°03′40″749 2
Riessersee N 47°28′47″ E 11°04′53″781 2
Griesen N 47°28′40″ E 10°56′27″824 3
Eibsee N 47°27′38″ E 10°59′14″982 1
Eibsee Alm N 47°27′16″ E 10° 59′34″1,011 1
Ehrwalder Alm N 47°23′17″ E 10°56′17″1,102 3
Ehrwald Zugspitzbahn N 47°25′36″ E 10°56′30″1,218 3

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Pca divided by the numbers of flowers per catkin (Flca). The
number of pollen grains per volume unit (1 m3) of crown
(Pvuc) was determined by multiplying Pca with the ratio of
the number of catkins per crown sampling unit (Csu) and
the volume of the sampling unit (0.125 m3). In addition, the
number of flowers (Flvuc) and catkins (Cvuc) per volume unit
of crown was extrapolated.
Environmental data
To assess the influence of temperature on pollen production,
we positioned nine loggers with radiation shields (HOBO
Pro v2 U23-001, Onset, Bourne, MA, USA). Each logger
was set up at a height of 2m a.g.l. on the northern side of
one birch tree from one location, which recorded tempera-
ture at 10-min intervals from February 2020 until June 2021.
A new HOBO logger was installed at the location Griesen in
January 2021 as the previous one was lost, and no data were
available for this site until December 2020. The location’s
missing daily temperature data were interpolated applying
linear regression with daily temperatures and altitudes of the
other eight loggers. The root-mean-square errors (RMSE)
between predicted and observed daily mean temperature dur-
ing January until June 2021 were 1.2. The software package
HOBOware (Version 3.7.23; Onset, Bourne, Massachusetts,
USA) was used to download the data from the loggers and
to export the raw data as text files.
We focussed on temperatures measured in the summer
previous of flowering, since this period is assumed to be
important for pollen production (Ranpal etal. 2022), as cat-
kins already start to develop and elongate (Dahl and Strand-
hede 1996). Thus, we were able to compare temperature
data of 2020 with pollen production of 2021. For the first
study year, we cannot resort to 2019 data; thus, we link pol-
len production of 2020 to March temperatures of 2020. For
comparison, we also link 2021 pollen data to 2021 March
temperatures.
Furthermore, we calculated growing degree-days (GDD;
in °C) of summer 2020 (June–August) by cumulating posi-
tive differences between the daily mean temperature (derived
as an average of Tmax and Tmin) and a threshold temperature.
In our study, we used a base temperature of 5°C (Bucher
etal. 2018; Estrella and Menzel 2006).
Statistical analyses
All levels of flower, catkin and pollen production were
checked for normality using Shapiro–Wilk test, which
revealed that these reproductive measures were not nor-
mally distributed. Non-normality was dealt with by using
non-parametric tests.
We examined differences between sampling years using
the non-parametric Mann–Whitney U test and applied
Spearman’s correlations to analyse association between
altitude and reproductive metrics. In addition, the influ-
ence of the altitude on the tree-specific differences in
reproductive metrics between 2021 and 2020 was checked.
To investigate the effect of environmental factors on pol-
len production of birch along the elevational gradient, we
compared reproductive metrics with temperature variables
(Tmean, Tmin, Tmax, GDD).
All statistical analyses were carried out withR version
4.2.2 (R Core Team 2020).
Results
Pollen, flowers andcatkins production
Pollen production per catkin (Pca) for all selected 17 birch
trees in the area of Garmisch-Partenkirchen was 5.23 ± 1.52
million pollen grains in 2020 and 2.51 ± 1.23 million pol-
len grains in 2021 (see Table2). Pca varied within a wide
range from approx. 400,000 (minimum of 2021) to 8.3 mil-
lion pollen grains (maximum of 2020). Pca in 2021 was
52% lower compared to 2020 when regarding mean values.
The number of catkins in a crown sampling unit (Csu; 0.125
m3) ranged between 1 (minimum of 2021) and 50 (maxi-
mum of 2020) with an average of 28 catkins in 2020 and
5 catkins in 2021 (− 82%). In addition, all other estimated
parameters, i.e. pollen production per flower (Pfl), per vol-
ume unit of crown (Pvuc) and the number of flowers per
catkin (Flca), were consistently higher in 2020, which does
not only apply to mean, but also to minimum and maximum
values (Table2).
Year‑to‑year variation inreproductive metrics
The Mann–Whitney U test revealed that the means of all
reproductive metrics except for flowers per catkin (Flca)
(p = 0.214) were significantly different between 2020 and
2021. In each case, the percentage change was positive, i.e.
the highest values were measured in 2020. Figure3 shows
exemplary the differences of Pfl, Pca, Pvuc, Flca, Flvuc and Cvuc
between 2020 and 2021.
Effects ofaltitude andtemperature onreproductive
metrics
Altitude
In 2020, there were no significant correlations between the
reproductive metrics and altitude (Table3). In 2021, some
correlation coefficients increased in magnitude, but were
not statistically significant (marginally significant for Flvuc,
rs = − 0.446, p = 0.073 and Cvuc, rs = − 0.443, p = 0.075).

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Figure4 illustrates the relationship between altitude and
reproductive metrics estimated in 2020 and 2021. Espe-
cially in 2020, but also in 2021, there is a large scattering,
which was also reflected by the non-significant relationship
(Table3). Regression lines were added in case of marginally
significant relationships.
Table 2 Descriptive statistics of pollen production per flower (Pfl),
per catkin (Pca) and per volume unit of crown (Pvuc); flower produc-
tion per catkin (Fca) and per volume unit of crown (Flvuc) and catkin
production per crown sampling unit (Csu; 0.125 m3) and per volume
unit of crown (Cvuc) estimated for 17 selected birch trees along an
altitudinal gradient in the Garmisch-Partenkirchen area during 2020–
2021. The second last column indicates the results of the Mann–
Whitney U test for comparison of means
Reproductive
metric Year Minimum Maximum Mean Median Standard devia-
tion W statistic (p value) Difference
2020 to 2021
(in %)
Pollen production
Pfl2020 20,442 79,007 45,738 44,886 13,041 256 (≤ 0.001) 48%
2021 4,445 56,139 23,639 23,154 12,798
Pca 2020 2,197,500 8,257,667 5,228,025 5,255,750 1,521,924 262 (≤ 0.001) 52%
2021 398,667 5,409,250 2,507,427 2,412,500 1,230,822
Pvuc 2020 187,620,000 2,039,200,000 1,095,620,550 929,480,000 562,490,982 287 (≤ 0.001) 91%
2021 6,378,672 482,500,000 96,997,804 69,294,000 109,138,708
Flower production
Flca 2020 84 146 115 114 16 181 (0.214) 6%
2021 77 125 108 112 14
Flvuc 2020 4560 42,560 25,163 24,240 12,085 278 (≤ 0.001) 82%
2021 896 20,800 4314 2712 4800
Catkin production
Csu 2020 5 50 28 25 14 276 (≤ 0.001) 82%
2021 1 25 5 3 6
Cvuc 2020 40 400 223 200 108 276 (≤ 0.001) 82%
2021 8 200 41 24 46
Fig. 3 Boxplots based on (a) Pfl, (b) Pca, (c) Pvuc, (d) Flca, (e) Flvuc
and (f) Cvuc estimated for 17 trees along an altitudinal gradient in
the Garmisch-Partenkirchen area for 2020 and 2021. The interquar-
tile range (IQR) is represented by the height of the boxes, maximum
and minimum values by the upper and lower whiskers, the median by
bold horizontal lines in the boxes, dots represent observations exceed-
ing or falling below 1.5 times the IQR

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Table 3 Spearman’s correlations between altitudes, temperature metrics, and reproductive metrics of 17 birch trees located in the Garmisch-Partenkirchen area in 2020 and 2021. rs Spearman’s
correlation coefficient, p significance value
Significant at the 0.05 level (bold values) and marginally significant (at the 0.1 level; italics values)
2020 Altitude Tmin March 2020 Tmean March 2020 Tmax March 2020 GDD March 2020
Pflrs − 0.071 0.093 − 0.006 − 0.014 − 0.009
p0.786 0.723 0.981 0.959 0.974
Pca rs − 0.148 0.190 0.087 0.059 0.020
p0.570 0.464 0.741 0.821 0.940
Pvuc rs − 0.221 0.085 0.117 0.068 0.209
p0.395 0.745 0.654 0.795 0.421
Flca rs0.122 − 0.170 − 0.138 − 0.157 − 0.185
p0.642 0.515 0.599 0.546 0.478
Flvuc rs − 0.104 − 0.049 0.030 − 0.020 0.022
p0.691 0.851 0.910 0.940 0.932
Cvuc rs − 0.165 0.006 0.078 0.031 0.068
p0.527 0.981 0.765 0.906 0.794
2021 Altitude Tmin March 2021 Tmean March 2021 Tmax March 2021 GDD March 2021 Tmin Summer 2020 Tmean Sum-
mer 2020
Tmax Summer 2020 GDD
Sum-
mer
2020
Pflrs0.405 − 0.147 − 0.234 − 0.189 0.115 − 0.288 − 0.399 − 0.328 − 0.330
p0.107 0.573 0.367 0.467 0.660 0.262 0.112 0.199 0.196
Pca rs0.363 − 0.119 − 0.220 − 0.171 0.121 − 0.279 − 0.354 − 0.289 − 0.289
p0.152 0.650 0.396 0.513 0.643 0.278 0.164 0.260 0.260
Pvuc rs − 0.303 0.361 0.512 0.455 0.774 0.504 0.232 − 0.010 0.272
p0.237 0.155 0.036 0.067 0.000 0.039 0.369 0.970 0.291
Flca rs − 0.032 0.170 0.133 0.100 0.159 − 0.004 0.101 0.224 0.153
p0.903 0.513 0.610 0.703 0.541 0.987 0.700 0.388 0.557
Flvuc rs − 0.446 0.470 0.635 0.509 0.650 0.613 0.391 0.173 0.425
p0.072 0.057 0.006 0.037 0.005 0.009 0.121 0.507 0.089
Cvuc rs − 0.443 Not shown since catkin development is prior to March 2021 0.642 0.400 0.145 0.425
p0.075 0.005 0.112 0.578 0.089

International Journal of Biometeorology
1 3
Figure5 demonstrates the differences in the selected
reproductive metrics (Pca, Flca and Cvuc) between 2020 and
2021. Though the correlations are all non-significant, some
interesting patterns can be revealed: Only two trees, located
above 1100m a.s.l., were linked to a negative Pca value, i.e.
higher pollen production, in 2021 (Fig.5a). Three trees at
the highest location (Ehrwald Zugspitzbahn; EZ) showed
relatively small differences, but two trees at Ehrwalder Alm
(EA) the largest differences. No or avery small differences
in Flca between 2020 and 2021 wereobtained for trees at
Alpspitzbahn (AB; 749m a.s.l.) and Kurpark (KP; 696m
a.s.l.). Four trees were linked to less flowers in 2021, the rest
to more flowers. A clearer pattern was seen for the differ-
ences in Cvuc between 2020 and 2021. Here, only one tree
(located at Riessersee; RS) was associated to a lower number
of catkins in 2020. However, correlation analyses revealed
no significant relation to altitude.
Temperature
In general, mean summer temperatures (June–August 2020)
recorded at each site were negatively and strongly correlated
Fig. 4 Scatterplots of altitude and Pfl in 2020 (a), 2021 (b); Pca in
2020 (c), 2021 (d); Pvuc in 2020 (e), 2021 (f); Flca in 2020 (g), 2021
(h); Flvuc in 2020 (i), 2021 (j); and Cvuc in 2020 (k), 2021 (l) esti-
mated for 17 trees in the Garmisch-Partenkirchen area. Regression
lines were added in case of marginally significant relationships
Fig. 5 Scatterplots of the difference in the selected reproductive met-
rics (a) Pca, (b) Flca and (c) Cvuc between 2020 and 2021 estimated
for 17 trees in the Garmisch-Partenkirchen area (locations: AB, Alp-
spitzbahn; EA, Ehrwalder Alm; EZ, Ehrwald Zugspitzbahn; KP, Kur-
park; and RS, Riessersee) and respective altitudes

International Journal of Biometeorology
1 3
with altitude (rs = − 0.940, p < 0.001). GDD of the same
period was also negatively and strongly correlated with
altitude (rs = − 0.880, p < 0.001). The highest temperature
mean (17.8°C), considered for the period of June–August
2020, was measured at Hindenburg (706m a.s.l.), which is
one of the lowest locations of the study. The lowest mean
annual temperature (14.8°C) was recorded at the highest
site, at Ehrwald Zugspitzbahn (1218m a.s.l.) (Table1). The
sites with the highest (Hindenburg; 5.0°C) and the lowest
(Ehrwald Zugspitzbahn; 1.7°C) temperature mean recorded
in March 2020 were the same as mentioned above.
The relationships with reproduction metrics and tem-
perature variables (minimum, mean, maximum tempera-
ture and GDD) were not statistically significant in 2020,
the year in which the highest pollen and catkin production
was observed. For 2021, however, we found some significant
correlations. Cvuc was significantly (p = 0.005) correlated to
summer Tmin (rs = 0.642). Since the amount of catkins in
a sampling volume also influences the reproduction meas-
ures Flvuc and Pvuc, positive and significant relationships
were also derived in these cases: Flvuc and summer Tmin
(rs = 0.613, p = 0.009), Pvuc and summer Tmin (rs = 0.504,
p = 0.039). Interestingly, other temperature variables calcu-
lated for the period June to August (mean and maximum
temperatures, GDD) were not significantly associated to
any of the reproductive metrics. Instead, March tempera-
tures were sometimes superior in describing the relationship.
The highest correlation was achieved with Pvuc and GDD
(rs = 0.774, p = 0.000). In summary, warmer conditions were
related to higher pollen and flower production, which was
only obvious for higher levels, i.e. for the volume unit of the
crown, as a result of the temperature dependency of catkin
numbers in 2021.
For visualization (Fig.6), we focused on the relationships
with reproductive metrics estimated in 2021 and minimum
summer temperature in 2020. The subplots (a), (b) and (d)
in Fig.6 demonstrate that pollen and flower production of
male inflorescences in 2021 was random with respect to the
Tmin of the previous summer. However, an increase in the
number of pollen, flowers and catkins per volume unit of
crown was observed with higher values of Tmin in summer
2020 (Fig.6c, e, f).
Discussion
The value ofgradient studies inpollen research
Long-term studies can profit from almost constant site con-
ditions (soil type, edaphic regime) and varying meteorologi-
cal conditions across years that may allow for calculating
trends or response rates based on the same individual and
therefore excluding genetic variability (Jochner etal. 2013a).
Studies along altitudinal gradients can be affected by several
factors such as complex environmental heterogeneity and
extreme geography (Körner 2007). As the space-for-time
approach also includes a multitude of different individuals
at various sites, differences in local environmental factors,
e.g. soil conditions, nutrient availability and water supply
as well as differences in pollution or other factors related to
local climate and genetics might exert additional influences.
Thus, gradient studies do not only account for differences in
Fig. 6 Relationship between (a) Pfl 2021, (b) Pca 2021, (c) Pvuc 2021, (d) Flca 2021, (e) Flvuc 2021 and (f) Cvuc 2021, and summer Tmin of 2020
for 17 birches along the altitudinal gradient in the Garmisch-Partenkirchen area. Regression lines were added in case of significant relationships

International Journal of Biometeorology
1 3
temperature, which is, however, the most important variable
when the effect of climate change is aimed to be assessed.
Pollen, flowers andcatkins production
In the present study, we investigated how reproductive met-
rics of Betula pubescens trees differ in 2 consecutive years
along an altitudinal gradient in the Bavarian Alps. We esti-
mated mean pollen production values at the level of catkins
ranging between 5 and 2.5 million. This estimate is com-
parable to that published by Erdtman (1954), who reported
a value of 6 million pollen grains per inflorescence for B.
pubescens. Our mean value, however, is an average of the
estimates from 17 downy birch trees growing in various
elevations for 2years (n = 34). According to Ranpal etal.
(2022), a catkin from Betula pendula (silver birch) produces
on average 1.7 million pollen grains. Such estimations of
pollen production might be important to assist pollen emis-
sion parameterization since commonly, their proxies were
only related to plant characteristics such as leaf area index
and canopy height (Helbig etal. 2004).
Estimation of pollen production by counting all pollen on
microscope slides is a labour- and time-intensive method.
Improved pollen counting methods, such as a cell counter
(Kakui etal. 2020) or automatic identification of the num-
ber of pollen grains on microscopic slides (Kadaikar etal.
2019), would make the method more efficient.
Year‑to‑year variation inreproductive metrics
The year 2020 was found to be a pollen- and catkin-rich year:
We estimated on average 109% more pollen grains per catkin
than in the following year. In addition, the number of catkins
per volume unit of crown was 460% higher in 2020, but
the number of flowers per catkin was only changed slightly
(+ 6%) and associated to a non-significant difference.
Flower numbers were not substantially different between
years. The number of anthers per flower is genetically fixed
and does not vary substantially (Fernández-González etal.
2020; Hidalgo etal. 1999; Subba Reddi and Reddi 1986).
In the case of birch, flowers per catkin seem to have the
most homogenous value among clones and years (Ranpal
etal. 2022). However, the number of flowers per volume unit
of crown was also calculated by multiplying the number of
flowers of single catkins by the abundance of catkins within
the volume. Thus, the number of catkins, which can largely
differ between trees and years, is the most decisive factor for
the value obtained for flowers per volume unit of a crown.
In general, reproductive metrics in birch trees can vary
greatly from year to year, as found by Jato etal. (2007),
Damialis etal. (2011) and Ranpal etal. (2022). Alternat-
ing patterns of flower (and seed) production are related to
masting behaviour, an inherent common feature in temperate
tree species that occurs, in the case of birch, every second or
third year (Detandt and Nolard 2000; Latałowa etal. 2002).
Given that the catkin (more than 10 times) and pollen pro-
duction (3 times) were extraordinarily high in 2020, one
may assume that this year was a masting year. At a seed
plantation in Baden-Württemberg, Germany (distance to
Garmisch-Partenkirchen approx. 210km), Ranpal etal.
(2022) also found that mean Csu of a total of 28 trees in 2020
was two times higher than in the preceding year and the sub-
sequent year. Data obtained from our pollen monitoring site
in Eichstätt, Bavaria (distance to Garmisch-Partenkirchen
approx. 160km), also indicated that 2020 was linked to a
high pollen load in the air: Here, an APIn (annual pollen
integral) of 8720 pollen grains*day/m3 was measured, com-
pared to only 1923 pollen grains*day/m3 in the following
year (unpublished data). In general, for defining mast years,
a longer time-series would be needed for a detailed iden-
tification and evaluation (LaMontagne and Boutin 2009).
The delineation of mast years is mostly based on concepts
that include the coefficient of variation that accounts for the
mean and standard deviation, but consistent and generally
applicable methods are not available (LaMontagne and Bou-
tin 2009). In the case of pollen, one reason might be the
underrepresentation of studies addressing flower masting
(Pearse etal. 2016; Satake and Iwasa 2002).
Thus, the lack of studies related to flower masting along
altitudinal gradients is not surprising. This is in contrast to
seed masting, where changes of temporal patterns of mast-
ing were inter alia already linked to the variation in climatic
conditions along elevational gradients (Masaki etal. 2020).
The authors found that mean fruiting density and fruiting
frequency of Quercus crispula decreased with elevation,
while the annual variation in fruiting density increased.
Therefore, harsh environmental conditions (e.g. low tem-
peratures) at high elevations might be linked to a reduced
photosynthetic production and increased masting (Masaki
etal. 2020). In our study, which was only based on two con-
secutive years, we found no significant dependency between
the deviation from 2020 and 2021 in pollen, flower or catkin
production and altitude (Fig.5). In 2020, the vast majority
of selected trees synchronously produced a higher amount
of pollen, flowers and catkins. However, it was obvious that
two trees located at high elevations were the only exceptions
showing a negative deviation (i.e. higher flower and pol-
len production per catkins in 2021). The number of catkins
produced in 2021 for those trees, however, was very low as
well; thus, the pollen or flower production based on larger
units (i.e. volume unit of the crown) was still higher in 2020.
These findings also point to the need for defining and cat-
egorizing (flower) masting since reproductive metrics can be
altered differently. For this reason, a larger dataset including
more observation years and more birch trees, e.g. located at
even harsher sites, would be desirable.

International Journal of Biometeorology
1 3
It should be noted (but must remain unevaluated) that the
masting year has occurred (in 2020) after the year (2019)
with the highest temperature (7.9°C) and lowest precipita-
tion sum (1315mm), registered in Garmisch-Partenkirchen
in the period of 2019–2021. This also calls for the installa-
tion of a long-term monitoring in order to be able to under-
stand the influence of meteorology on masting years in more
detail.
Effects ofaltitude andtemperature onreproductive
metrics
Altitude
We found that there were no prominent changes in the ana-
lysed reproductive traits with increasing altitude (Table3;
Fig.4). The results of very few prior studies studying pol-
len production along altitudinal gradients showed that there
is no conclusive evidence on the associated relationships
with increased elevation since a decrease in pollen produc-
tion (Markgraf 1980; Moe 1998), an increase (Aguilera and
Valenzuela 2012) or no significant change (Charalampopou-
los etal. 2013; Hasegawa etal. 2022) was observed. Agu-
ilera and Valenzuela (2012) argued that higher olive pollen
production observed at elevated regions might be related
to intrinsic mechanisms of these trees to compensate for a
limited pollination efficiency and a shorter growing period.
However, these results may also be affected by human inter-
ventions (cutting) that may have a masking effect on pol-
len production. However, in some of the studied species at
Mount Olympos, pollen and inflorescence traits at the higher
reproduction level (e.g. per individual tree) were decreased
with increasing altitude (Charalampopoulos etal. 2013). In
this study, we decided not to integrate the number of pollen,
flowers or inflorescences per individual, since this meas-
ure is strongly dependent on the age and height of a tree
that considerably varies along the gradient under investiga-
tion. In addition, extrapolating production estimates to the
whole tree is based on the assumption of a simplified geo-
metric shape of the tree (Molina etal. 1996). However, this
potential geometric shape differs from its original form to a
certain extent, implying uncertainties in the estimation for
the level of an individual tree. All variables based on a spe-
cific volume are believed to be superior indicators of pollen
production, since they account for the pollen produced per
catkins and the number of catkins in a standard volume (1
m3). Some studies, such as those by Bogawski etal. (2019)
and Katz etal. (2020), have used LiDAR data to determine
crown parameters, which were used for estimating pollen
production per tree or tree stand.
The result of this study indicated that the number of
male inflorescences per crown sampling unit (Csu) in 2021
decreased along the gradient (rs = − 0.443, p = 0.075,
Table3). Thus, compensation for pollen limitation might
more strongly affect the pollen produced by single inflores-
cences. Fernández-González etal. (2020) found that smaller
sized tree species of the genus Quercus attempt to produce
a higher amount of pollen per anther to ensure fertilization.
Temperature
Although we found a strong and significant relation with
temperature and altitude, those variables associated to tem-
perature showed stronger and more significant correlations
than altitude alone. This also points to the fact that tempera-
ture measurement should be implemented in any altitudinal
gradient studies.
In 2021, we detected an increased catkin formation at
warmer (lower) locations, which was also reflected in the
reproductive metrics whose computations were based on the
number of catkins. Our results indicated that minimum tem-
perature was superior in any statistical analyses than mean
and maximum temperatures or even GDD.
Non-significant relationships with temperature were
found in 2020, the assumed mast year. The reason might
be that the amount of pollen and inflorescences produced
by the selected birch trees in our study was most probably
regulated by the resource balance of the trees, and mast-
ing-associated parameters masked other influences and
variability present in normal reproductive years. Accord-
ing to the resource budget model, masting can occur due to
plants’ resource balance even in the absence of interannual
environmental variations (Isagi etal. 1997). In general,
pollen concentration and therefore pollen availability is
reduced at higher elevations due to a decreasing preva-
lence of birch trees (Charalampopoulos etal. 2013; Joch-
ner etal. 2012). A lower availability of birch pollen might
also cause low seed production. Following the resource
storage hypothesis, this may affect resource accumulation
resulting in more flowering/fruiting (Bogdziewicz etal.
2020) as observed in our study in 2020. Therefore, the fact
that birch is only seldom represented at higher altitudes
in our study area, might also affect its resource budget,
which could mask the influence of environmental factors
such as temperature.
Existing studies indicate varying relationships between
temperature and pollen production. Jochner etal. (2013b)
found a significant reduction in pollen production per cat-
kin in silver birch (Betula pendula Roth) at urban locations
(under higher temperatures) in Munich (Germany). The
authors argued that conditions in urban areas might have a
negative effect on the physiology of birch and thus on pol-
len production. On the other hand, an urban gradient study
indicated that an increase in temperature increased the pol-
len production of other species such as common ragweed
(Ambrosia artemisiifolia, Ziska etal. 2003).

International Journal of Biometeorology
1 3
In general, microclimate is believed to have a strong
impact on pollen production (Aguilera and Valenzuela
2012); therefore, a variability is quite expected and would
be even more pronounced when studying a larger altitudinal
gradient. With the calculated temperature lapse rates in this
study (season-depended varying between 0.4 and 0.6°C;
not shown in the results section) and the given gradient of
522m, a temperature difference of 2.1 and 3.1°C might
be too low to observe strongeffectson pollen, flower and
inflorescence production.
Effects ofother environmental parameters
In addition, other information than air temperature might
be important: A study in alpine environments by Scherrer
etal. (2011) found significant fluctuations in soil tempera-
ture of up to 4°C depending on slope aspect and topography.
Because of this, even trees at the same location and similar
altitude are exposed to different microclimatic conditions
that might affect reproductive traits.
Air pollutants such as nitrogen dioxide (NO2) might
reduce (Jochner etal. 2013b) or increase pollen produc-
tion of birch (Zhao etal. 2017). In addition, ozone (O3)
was also found to affect birch reproduction (Darbah etal.
2008). Birch trees growing in areas with higher NO2 levels
were found to be more often affected with birch idaeovirus
(Gilles etal. 2023), and such biotic stress could further influ-
ence the reproduction of infected trees. These pollutants are
likely to change with increasing elevation and should also be
incorporated in further studies. In the present study, we only
measured NO2 and O3 during a 1-week period in late spring
2020 and found significant correlations between NO2 and
Pvuc 2020 (rs = 0.520, p = 0.032) as well as between O3 and
Pca 2020 (rs = − 0.519, p = 0.033) and Pfl 2020 (rs = − 0.489,
p = 0.047) (not shown). Since these results are only based on
a short measurement duration, we decided not to incorporate
these findings in the “Results” section but encourage fur-
ther research to specifically focus on pollution as potential
influential factor. Since the effects of pollution might also
be species-specific, there is also a strong need to compare
different plant species.
Moreover, other factors can have an influence on pol-
len production, such as artificial pruning/topping, since the
induction of stress results in a higher reproductive output
(Ranpal etal. 2022). In addition, site characteristics such as
stand density and exposure (Faegri etal. 1989) and genetics
(Ranpal etal. 2022) were found to be relevant in the discus-
sion on pollen production.
Knowledge derived from seed masting studies suggest
that nutrient availability which usually declines with eleva-
tion as a result of decreased organic matter decomposition
and nutrient mineralization (Sundqvist etal. 2013) might
also affect seed availability (Allen etal. 2014). Related to
birch pollen production per catkin, it was found that iron
concentration (assessed in birch leaves) was linked to a
decrease (Jochner etal. 2013b), but other information on
the influence on nutrients, specially assessed in the soil, is
largely lacking.
Low temperature and high moisture availability 2years
before seed fall was linked to a higher amount of seed pro-
duction (Richardson etal. 2005). Relationships with repro-
duction variables related to pollen based on lag effects, how-
ever, are not commonly evaluated in existing research and
highlights the need for long-term studies.
In addition, more experimental studies may be best
suited to disentangle the influence of temperature and other
factors influencing reproduction traits of plants and their
magnitude free from masked effects. Birch trees become
sexually mature (and bear male catkins) from the age of
approx. 10–15years (Perala and Alm 1990). Therefore, in
the case of birch, experimental setups remain challenging
since their relocation to laboratory conditions cannot easily
be materialized.
In summary, future research could benefit from the inclu-
sion of more birch trees spanning an even larger altitudinal
gradient and observation years. Ideally, a long-term monitor-
ing, which is still not established, is desirable. Spatial infor-
mation on air pollution along with meteorological measure-
ments is helpful to conclude on their influences on pollen
production. Less time-consuming methods of pollen quan-
tification should be tested and more experimental research
avoiding masked effects on pollen production is suggested.
Conclusions
In conclusion, this study provides valuable insights into the
production of birch pollen, flowers and inflorescences in
relation to thermal parameters across an elevational gradient.
The findings of this study indicate that no significant changes
in the reproductive traits were detectable with increasing
altitude alone. Moreover, likely due to the temperature
dependency of catkin numbers in 2021, warmer sites were
associated with higher pollen and flower production, which
was only apparent for higher levels, i.e. for the volume unit
of the crown. Temperatures further from the optimum of
birch growth might be linked to more pronounced changes;
thus, studying pollen production along even larger altitudinal
gradients is highly relevant in future research.
Acknowledgements We thank Miriam Sieverts, Verena Wörl, Anna
Katharina Zerhoch and Sabine Fürst for their support and technical
assistance.
Author contribution Conceptualization: Susanne Jochner-Oette.
Methodology: Susanne Jochner-Oette, Surendra Ranpal and Atha-
nasios Damialis. Software: Surendra Ranpal. Validation: Susanne

International Journal of Biometeorology
1 3
Jochner-Oette, Surendra Ranpal and Athanasios Damialis. Formal
analysis and investigation: Surendra Ranpal. Resources: Susanne
Jochner-Oette and Surendra Ranpal. Data curation: Surendra Ranpal.
Writing—original draft preparation: Surendra Ranpal. Writing—
review and editing: Surendra Ranpal, Susanne Jochner-Oette, Atha-
nasios Damialis, Stefanie Gilles, Daria Luschkova, Maria Landgraf,
Carmen Büttner, Claudia Traidl-Hoffmann and Susanne von Bargen.
Visualization: Surendra Ranpal. Supervision: Susanne Jochner-Oette
and Athanasios Damialis. Project administration: Susanne Jochner-
Oette. Funding acquisition: Susanne Jochner-Oette, Carmen Büttner,
Claudia Traidl-Hoffmann.
Funding Open Access funding enabled and organized by Projekt
DEAL. This research was funded by the German Research Founda-
tion (Deutsche Forschungsgemeinschaft) (DFG) as part of the pro-
ject “pollenPALS: Biotic and abiotic effects on pollen production and
allergenicity of birch and related health impacts (655850)”. The study
was partly implemented in the frame of the EU-COST Action ADOPT
(New approaches in detection of pathogens and aeroallergens), Grant
Number CA18226 (EU Framework Program Horizon 2020).
Declarations
Consent for publication All the authors have consented on their own
behalf for the publication of this study.
Competing interests The authors declare no competing interests.
Open Access This article is licensed under a Creative Commons Attri-
bution 4.0 International License, which permits use, sharing, adapta-
tion, distribution and reproduction in any medium or format, as long
as you give appropriate credit to the original author(s) and the source,
provide a link to the Creative Commons licence, and indicate if changes
were made. The images or other third party material in this article are
included in the article's Creative Commons licence, unless indicated
otherwise in a credit line to the material. If material is not included in
the article's Creative Commons licence and your intended use is not
permitted by statutory regulation or exceeds the permitted use, you will
need to obtain permission directly from the copyright holder. To view a
copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/.
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