Supporting Information Methods S1, Figs S1–S3, Tables S1–S6
Does humidity trigger tree phenology? Proposal for an air humidity based framework for bud
development in spring.
Julia Laube, Tim H. Sparks, Nicole Estrella & Annette Menzel
Methods S1
Experiment 1: Dormant cuttings (c. 25 cm length) of 9 different woody species (Table S1)
were cut on 03.03.2012 from a forest near Freising (Germany), cleaned and put into 0.1 l
glass bottles filled with tap water. For each species, 10 twigs (from 3 different trees) were
kept in a climate chamber with 40% RH (relative air humidity), 10 twigs in an identical
chamber with 90% RH for 30 d. To assure proper water supply, twigs were re-cut and water
was changed every 2nd week. The temperature program in both chambers started with day
19.5°C (1.5°C night reduction), and increased 0.5°C per day until 30.5°C (with 2.5°C night
reduction). Overall mean temperature was 25.3°C, photoperiod was 16 h daylight. The
development stages of buds were recorded using BBCH-codes (Meier, 2001) three times per
week. We analysed the time (number of days) until budburst for different phenophases
(budburst, mouse-ear stage, leaf unfolding) by linear mixed effect models (function lme, RPackage nlme, Pinheiro et al., 2012). Tests on single species included tree identity as a
random effect (tree identity nested within treatment). Treatment effect in the complete dataset
was assessed with tree identity and species as random effects (tree identity and species nested
within treatment). Normality assumptions were inspected via QQ-Plots, and in the case of
departures from normality, the results were confirmed by Kruskal-Wallis tests, with largely
comparable results (details not shown).
Table S1 Species used in the Experiments 1–3
Species
Scientific name
Division
Class
Family
Experiment
Aspen
Populus tremula L.
Magnoliophyta
Dilleniidae
Salicaceae
1,2,3
Beech
Fagus sylvatica L.
Magnoliophyta
Hamamelidae
Fagaceae
2
Birch
Betula pendula Roth.
Magnoliophyta
Hamamelidae
Betulaceae
1,3
Cornel
Cornus mas L.
Magnoliophyta
Rosidae
Cornaceae
1,3
Larch
Larix decidua Mill.
Pinophyta
Pinidae
Pinaceae
1,3
Lilac
Syringa vulgaris L.
Magnoliophyta
Asteridae
Oleaceae
1,3
Locust
Robinia pseudoacacia L.
Magnoliophyta
Rosidae
Fabaceae
1,3
1
Species
Scientific name
Division
Class
Family
Experiment
Oak
Quercus robur L.
Magnoliophyta
Hamamelidae
Fagaceae
1,2,3
Maple
Acer pseudoplatanus L.
Magnoliophyta
Rosidae
Aceraceae
2
Snowberry
Symphoricarpos albus L.
Magnoliophyta
Asteridae
Caprifoliaceae
1,3
Spruce
Picea abies (L.) H. Karst.
Pinophyta
Pinidae
Pinaceae
1,3
Experiment 2: Cuttings (c. 15 cm length) of 4 tree species (Table S1) were cut on 15.04.2012
(fully chilled), the cut was taped to prevent water uptake via vascular tissue. Twigs were put
in dry (empty) glasses within humid boxes (see Fig. S2). Development stages (Meier, 2001)
and weights of the twigs (moist weight) were recorded during 3 wk using an analytical
balance (Satorius, verification interval 1mg). One box was sprayed with water daily, the other
box had no additional spraying. Mean temperature was 22.6°C in both boxes, relative air
humidity was 99% and 94%, respectively, the number of replicates per box and species was
10. We analysed increase in mass with respect to phenological development using
nonparametric statistics, since normality assumptions were not met. We used Kruskal-Wallis
tests to assess the difference between treatments (spraying/non spraying), and rank correlation
to test the relation between weight increase and the development phase of twigs).
Analysis of winter/spring climate data: Daily climate data (1951–2009) of six meteorological
stations (see Fig. S1) were obtained from the German weather service. Stations were chosen
to represent the main climatic gradients in Germany (prealpine to coast, warm and humid
Rhine valley to continental and dry northeast). The smoothness of temperature and air
humidity increases during spring and summer was analysed. We used the coefficients of
variation (C.V.), based on the deseasonalised (subtraction of moving average) daily values per
year to judge the variability of the parameters. Significance of differences between absolute
humidity and temperature were tested using sign tests. We additionally analysed both
variables with respect to frost. Daily mean values of all stations and years were arranged
relative to the last cold day occurring in spring (cold days are days with mean temperature at
or below 0°C). We analysed the trend (slope) in daily values 60 d before and after the last
cold day. Significance levels were assessed by linear mixed effect models with years and
stations as covariates, and a first order autoregressive correlation structure to account for
autocorrelation of daily values (R package nlme, Pinheiro et al., 2012).
2
Fig. S1 Meteorological stations in Germany used for the calculation of the air humidity spring
signal.
Experiment 3: A third experiment with 3 chilling treatments investigated the phenological
development of twigs during a 6 wk forcing period. We used the same 9 species as in
experiment 1 (Table S1), and cut dormant twigs at different dates throughout winter. Cuttings
(10 replicates per species) were cleaned and put into 0.1 l glass bottles filled with tap water.
Picea abies was included only in intermediate and high chilling conditions (hence is missing
for the low chilling treatment). Different chilling treatments were achieved by different
lengths of exposure to natural (outdoor) chilling conditions (see Table S2). The development
stages of buds were recorded as in experiment 1 using BBCH-codes (Meier, 2001) three times
per week, the phenological development of donor trees in the field was recorded weekly. The
temperature program for all chilling treatments was identical, starting with 7°C and raised
0.5°C daily, until 27.5°C at the end of the experiment (end of week 6). Relative humidity was
held constant at around 70%. Night time reduction of temperatures began at 11°C (day 11°C,
night 9°C) and was gradually raised to a difference of 5°C day/night (12 h/12 h). For the first
chilling treatment, the limited experimental period of 6 wk led to right-censored data, that is,
not all twigs had developed to budburst within the treatment period. Hence medians were
calculated as Kaplan-Meier survival estimates (R-Package Survival, Therneau, 2013). To
3
analyse the effects of chilling we used total forcing sums up to the dates of budburst. The total
forcing sum was calculated from the forcing sums received during experimental and under
field conditions, formulas for the calculation of thermal and humidity forcing sums are given
in Table S3. The analysis included median forcing sums per species of experiment 1 (with
101 chill days) and medians per species and treatment in experiment 3 (33, 73, and 110 chill
days), as well as median budburst dates observed in the field (with up to 116 chill days
depending on species). Field climate data were obtained from the German weather service, the
climate station was c. 2 km from the field sites.
Table S2 Description of the different chilling treatments (Experiment 3). Chill days are given
as the number of days since November 1st with mean temperatures below 5°C (Murray et al.,
1989). Thermal time and humidity time received under field conditions by the start of
experiments were calculated as given in Table S3. Budburst in the field occurred between
28.03.2012 and 09.05.2012, hence the number of chill days varies between species.
Start of
Number of chill
Thermal time
Humidity time
experiment
days
(°C days)
(g m-3 days)
Chilling 1 (experiment 3)
14.12.2011
33
0
0
Chilling 2 (experiment 3)
30.01.2012
73
63.9
142.8
Humidity experiment (experiment 1)
03.03.2012
101
114.5
263.2
Chilling 3 (experiment 3)
14.03.2012
110
155.5
321.0
-
110-116
206.0-676.7
358.7-674.8
Treatment
Field observations
Table S3 Formulas for chill days, thermal time and humidity time. RCT, rate of chilling; T,
mean daily air temperature; Tc, threshold of chilling value (set to 5°C); tc, starting date of
chilling accumulation, set to 1st November; t1, onset date; RF, rate of forcing; F, forcing
value (either mean daily temperature or mean daily absolute air humidity); Ft, threshold of
forcing value (only for temperature, set to 0°C); SFcrit, critical forcing sum; tf, starting date of
forcing accumulation, set to 1st January; t1, onset date.
0,
𝑓𝑜𝑟 𝑇 > 𝑇𝑐
𝑅𝐶𝑇 = {
1,
𝑓𝑜𝑟 𝑇 ≤ 𝑇𝑐
𝑡1
𝑆𝑢𝑚 𝐶ℎ𝑖𝑙𝑙𝑑𝑎𝑦 = ∑ 𝑅𝐶 𝑇
𝑡𝑐
Source (Murray et
al., 1989)
Source (Murray et
al., 1989)
4
0,
𝑓𝑜𝑟 𝐹 ≤ 𝐹𝑡
𝑅𝐹 = {
𝐹 − 𝐹𝑡 ,
𝑡1
𝑆𝐹𝑐𝑟𝑖𝑡 = ∑ 𝑅𝐹
𝑡𝑓
𝑓𝑜𝑟 𝐹 > 𝐹𝑡
Source (Kramer,
1994)
Source (Kramer,
1994)
5
Figures
Fig. S2 Twigs at the (a) beginning and (b) end of experiment 2.
Fig. S3 Increase of (a) temperature and (b) absolute air humidity during winter and spring.
The mean day for last cold day is DOY 74 (mid March), hence the period shown mostly
ranges from mid November to mid July (relative day –120 to 120) or mid January to mid May
(relative day –60 to 60). N = 336 (6 stations as given in Fig. S1, all years, except when cold
day was missing).
For the period 120 to 60 d before last cold day, both mean daily humidity and temperature
values show a decline.
For the period from 60 to 1 d before the last cold day the temperature already increases
significantly (slope b=0.010, P=0.025), while no trend exists for humidity (b=-0.002,
P=0.165). After the last cold day both variables show a positive trend. With respect to
temperature this implies the reinforcement of an existing trend (after the last cold day:
b=0.129, P<0.001), while for absolute humidity this represents the emergence of a new trend
6
(after the last cold day: b=0.042, P<0.001).These figures suggest that the air humidity spring
signal marks the end of cold days more clearly than the temperature spring signal.
Table S4 Effect of air humidity treatments on time (days) to reach phenological phases in
experiment 1. Values were assessed by linear mixed effect models with tree identity as a
random factor. Given are the degrees of freedom (df), intercept (Int) and treatment (Treat)
coefficients, with the dry 40% relative humidity chamber as baseline, as well as the
significance level (P), with bold: P<0.05. When QQ-Plots suggested departures from
normality assumptions, significant results were confirmed by Kruskal-Wallis tests. Scientific
species names are given in Table S1.
Days to budburst
Days to mouse-ear stage
Days to leaf unfolding
Species
df
Int
Treat
P
df
Int
Treat
P
df
Int
Treat
P
Aspen
16
12.7
-1.9
0.002
16
15.7
-3.3
<0.001
16
17.8
-2.7
0.054
Birch
16
6.0
0.1
0.922
16
10.5
-1.5
0.044
15
11.8
-2.1
0.020
Cornel
16
7.6
-0.3
0.562
16
11.4
-2.1
0.030
13
23.1
-11.4
<0.001
Larch
16
5.3
-0.3
0.689
16
9.4
-1.7
0.058
16
14.3
-5.0
<0.001
Lilac
16
4.0
0.2
0.328
16
11.7
-3.6
0.059
13
19.4
-7.9
0.019
Locust
15
11.2
-3.8
0.009
15
16.2
-6.6
<0.001
14
29.1
-4.1
0.008
Oak
16
17.9
-1.7
0.017
15
20.7
-0.6
0.526
14
24.3
-1.1
0.415
Snowberry
16
4.5
-0.5
0.328
16
8.3
0.4
0.510
16
15.1
-4.1
0.055
Spruce
12
17.0
-0.3
0.855
11
21.8
0.6
0.668
11
24.2
0.4
0.770
7
Table S5 How is water transported to developing buds in early spring?
Results reported in former studies
Comments
Bud water
Bud water content decreases in autumn and winter, Thus buds in development need water, and authors
content
while non-lethal losses of up to 75% have been agree that it needs to be transported to the buds.
changes
reported (Burström, 1948a). In spring and with
relation to bud development, a strong increase in
water contents occurs (West & Salo, 1979;
Essiamah & Eschrich, 1986; Rinne et al., 1994;
Welling et al., 2004). Water content increase is
supposed to be amongst the most important factors
during bud development (de Fay et al., 2000;
Yooyongwech et al., 2008).
Timing of bud
Initial growth and changes in bud structures often The first macroscopical change in bud development
water demands
occur already 3 wk before any macroscopic change occurs with onset of bud swelling, which itself takes
is visible. At that time also bud respiration starts to at least 1 wk, sometimes up to 3 wk (personal
increase (Burström, 1948b; Essiamah & Eschrich, observation, also (Fonti et al., 2007)). Hence the start
1986; McPherson et al., 1997).
of water supply to buds must be expected to occur
considerably (at least one month, up to 6 wk) before
budburst.
Water transport
Relocation of
Water content increase in Salix-catkin buds in Also stems and twigs dehydrate highly during winter
stored water
Alaska is reported to occur considerably before the (Welling
&
Palva,
2006).
Hence
it
seems
end of severe soil frost. The increase in water questionable if highly dehydrated tissue is able to
contents of buds is suggested to originate from release and translocate reasonable amounts of water.
storage pools within the stem (West & Salo, 1979).
Changed water
Water movement/mobility and dormancy are We do not doubt that a rising proportion of unbound
mobility
related (Kalcsits et al., 2009; Tanino et al., 2010). water contributes to bud water demands, but it seems
The proportion of unbound (free) water within questionable if the amount of “freed water” is
fully chilled buds increases with the state of sufficient. Water content increases during bud
forcing, while the proportion of non-available, development are often close to or above 100%
bound water decreases (Erez et al., 1998; (Burström, 1948b; West & Salo, 1979; Essiamah &
Parmentier et al., 1998). This contributes to bud Eschrich, 1986; Welling et al., 2004), indicating that
development.
a net transport of water into the buds occurs during
development.
Vascular
Xylem embolism increases during winter, the Not only reduced xylem flow rates, but also the
transport
maximum of cavitation is reported to occur shortly absence of connecting structures from bud to twig
before budburst. Xylem embolism is caused by should hamper water supply via xylem, since at the
freeze-thaw events, and heavily reduces hydraulic beginning of bud development and growth, no
conductance in early spring (de Fay et al., 2000; vessels exist (Burström, 1948a; de Fay et al., 2000).
Cochard et al., 2001; Cruiziat et al., 2002; Nardini Vessel growth within buds occurs parallel (and not
et al., 2011).
prior) to bud growth and development (de Fay et al.,
2000).
8
Results reported in former studies
Comments
Xylem recovery and onset of xylem transport in Thus newly grown vessels should contribute to bud
early spring are possible due to growth of new water supply only during advanced stages of bud
vessels (Cochard et al., 2001). Growth of new development.
vessels and cambial reactivation is usually
reported to start at or soon after budburst (Cochard
et al., 2001; Fonti et al., 2007; Cufar et al., 2008;
Cuny et al., 2012), but see (de Fay et al., 2000).
During spring, trees develop root and stem Regardless of hydraulic questions the timing of stem
pressure which transports water upwards (Cochard pressure development with respect to budburst also
et al., 2001; Miller-Rushing & Primack, 2008). It seems vague: Recovery of xylem embolism, root
is still under debate whether stem and root pressure and budburst (Essiamah & Eschrich, 1986;
pressure are strong enough to explain bleeding and Strati et al., 2003) or leaf unfolding (Cochard et al.,
xylem recovery (Cochard et al., 2001; Westhoff et 2001)
are
reported
to
occur
simultaneously.
al., 2008). Nevertheless, sap flow and embolism However, if the water demands of early bud
recovery are reported to influence leaf unfolding development are to be fulfilled, root/stem pressure
(Cochard et al., 2001), and also budburst is related and xylem recovery should advance budburst for
to the timing of root pressure development (Strati several (at least 4) wk. Such a time lag has not been
et al., 2003).
Other
reported.
It has been proposed that water vapour transport
also contributes to xylem recovery (Zwieniecki &
Holbrook, 2009). This seems possible since at
least summer foliage water uptake is able to
increase stem water potential (Boucher et al.,
1995), and can even reach levels that reverse
xylem sap flow towards the roots (Burgess &
Dawson, 2004).
Conclusion
An overall explanation of water transport to buds during initial development stages is not trivial. If
structural changes and growth in buds occur about 4 wk before budburst, then stem or root pressure might
only contribute partially. If we take into account that not only buds, but also twigs and stems are highly
dehydrated, high amounts of water translocation from nearby tissue seem unlikely. As winter embolism
reduces xylem transport heavily, an exclusive water supply via the stem is also questionable, since the
onset of xylem transport seems not to coincide with the water demands of early bud development.
Additionally, the amount of water transported upwards (regardless if transported within phloem or within
the remaining, uncavitated xylem vessels) should meet the water demands for rehydration of bark and
wood, full xylem recovery, onset of transpiration and bud development simultaneously. Thus spring might
not only be harsh with respect to a danger of frost, but also with respect to imperfect water supply, at least
if crowns of trees are considered.
The ability of foliar water uptake seems to be widespread among taxonomical groups (Limm et al., 2009),
and might act as an additional source of water during spring, when the primary water supply via the stem
is still hampered.
9
Table S6 Are buds and twigs capable of uptaking water from the air?
Results reported in former studies
Bud contents
Comments
Usually in buds and twigs, starch content increases during At the end of winter, buds and twigs have
summer and autumn, and decreases during winter. The highly dehydrated tissue that contains large
decomposition of starch to sugars contributes to frost amounts of hydrophilic substances. We hence
tolerance (Rinne et al., 1994; Welling & Palva, 2006). would expect high water potential differences
Also sugar concentrations of twig xylem increase during between these tissues and the surrounding air.
winter (Sakr et al., 2003). Highest sugar content is found
before budburst (Lipavska et al., 2000). Not only sugars,
but also other, strong hydrophilic substances are found in
buds before budburst (Welling & Palva, 2006; Kalcsits et
al., 2009). Dehydrins increase during winter and decrease
during early spring (Welling et al., 2004).
Amongst other factors, frost hardiness is attributed to
tissue dehydration. During autumn and winter, a strong
decrease in water content of buds and twigs is common,
followed by drastic water content increase before budburst
(West & Salo, 1979; Essiamah & Eschrich, 1986; Rinne et
al., 1994; de Fay et al., 2000; Welling et al., 2004;
Yooyongwech et al., 2008).
Stomata
During winter, ABA concentrations increase, followed by ABA is known to induce dormancy and cause
a sharp decrease before budburst (Rinne et al., 1994; stomata closure. It seems likely that stomata
Welling & Palva, 2006). Budburst is related to both ABA of young leaves (within the bud), bud scales,
decrease and water content increase (Rinne et al., 1994).
and twigs are closed during winter, while
Stomata activity and the ability to open to maximum both a decrease in ABA content and increased
follow a strict internal rhythm, which is independent of stomata activity might promote stomata
external factors. Minimum stomata activity is reported to opening in spring.
occur during winter, while afterwards (during early spring)
a sharp increase in ability to open fully is reported
(Seidman & Riggan, 1968).
Water vapour rather than fluid water is suggested to be It seems possible that increasing humidity
responsible for stomatal responses (Peak & Mott, 2011), during early spring triggers stomata opening.
and water vapour also increases stomatal conductance Thus water vapour exchange between twigs,
(Boucher et al., 1995).
young leaves and to a lesser extent also bud
Stomata occur at all aerial parts of the plant body (such as scales
with
stems and leaves) (Hetherington & Woodward, 2003), the promoted.
highest density of stomata is found on leaves in young
buds
(Kozlowski
&
Pallardy,
1997).
Bud
scales
(cataphylls) have fewer stomata than leaves, or no stomata
at all (Romberger et al., 1993). Foliar water uptake is
proposed to occur, amongst others, also via stomata
(Slatyer, 1960).
10
surrounding
air
might
be
Results reported in former studies
Epidermis
Comments
Foliar water uptake via cuticula can deliver amounts of As bud scales do not seem to prevent
water sufficient to increase leaf water potential noticeably. transpiration considerably better than normal
The rates of cuticular uptake increase with the presence of leaf cuticula, it seems likely that a water
cracks or abrasion at cuticles (Kerstiens, 1996; Burgess & exchange in the reverse direction should be
Dawson, 2004). Water uptake even via thick wax cuticles comparable to that of leaves. At the end of
is possible (Burgess & Dawson, 2004). Bud scales are winter and early spring, mechanical damage
usually very thin (often only one row of cells (Romberger is likely, which might further contribute to
et al., 1993)), and their capacity to insulate against permeability of bud scales.
transpiration loss is shown to be comparable to cuticles of
ordinary leaves (Burström, 1948a).
Bud water
Dry, dormant buds are able to absorb water vapour from Only endodormant buds were examined. If
uptake
the air (Burström, 1948a; Wolter & Kozlowski, 1964). As the highly increased activity of stomata,
absorption rates reached only 30% of transpiration rates, higher amounts of hydrophilic contents and
this ability was suggested to be of little ecological probably increased cuticular uptake due to
significance (Burström, 1948a).
damage in bud scales are taken into account,
absorption rates of ecodormant buds in early
Diurnal variations of bud water contents can, amongst spring should exceed the reported rates
others, be attributed to bud transpiration and moisture considerably. Additionally, not only buds but
uptake from the atmosphere (Kozlowski & Petersen, also twigs seem to be involved in uptake
1960).
Conclusion
(Burström, 1948a).
In early spring, aboveground tissue is highly dehydrated and filled with considerable amounts of
hydrophilic substances. This would raise the expectation that strong water pressure tension differences
occur between tissue and surroundings. Simultaneously, a high number of stomata within and at the
budscale, twig and stem quickly regain full activity, and thus might contribute considerably to uptake of
water vapour. Thin and possibly injured bud scales, not fully developed cuticula of young leaves within the
buds, and bark might also absorb water. Besides uptake processes, also purely mechanical effects might
contribute to an advance in bud development. Albeit no former studies were found on this point, it seems
possible that moist air results in softening of bud scales and hence facilitate bud swelling and splitting.
Orchards have used oil sprays for decades to delay budburst and hence reduce frost damage (Myers et al.,
1996; Dami & Beam, 2004). The physiological reason for this is not well understood, reduced respiration
or increased CO2 levels within the tissue are suggested to produce this effect. It might also be attributed to
limited uptake of water.
11
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