The Dynamics of the Phenological Development of Four Woody Species in South-West and Central Slovakia

Phenological observations record the dynamics of vegetation in relation to meteorological conditions as well as the long-term trends in relation to climate change. We processed 20-year data of the flowering (BBCH scale 60), leaves unfolding (BBCH 11) and ripening of fruits (BBCH 86) of four woody species in south-west and central Slovakia. The phenological year begins with the flowering of the hazel. This phenophase has the largest amplitude of onset (52–65 days) as well as interannual variability (sx = 20.2–33.4%) as it enters an unstable condition in early spring. At all stations, the order of phenophases is the same from the end of April. We found the highest vertical phenology gradient of the BBCH 60 Tilia cordata Mill. (6 days/100 m) and the smallest of BBCH 11 T. cordata (2.4 days/100). The statistically significant trends (p < 0.05) in shifting to the earlier period were in BBCH 60 Crataegus oxyacantha L. (0.4–0.5 days per year), BBCH 86 Corylus avellana L. (0.6 days per year), BBCH 60 Prunus spinosa L. (0.5–0,6 days per year) and BBCH 11 Prunus spinosa L. (0.6–0.7 days per year). These shifts indicate the change in the onset of the phenophases in south-west and central Slovakia.


Introduction
Phenology, together with the object of its study, is the basis for understanding ecological relationships in natural and modified systems on which human society is dependent [1,2].Many studies have shown that climate change with rising temperature causes the prolongation of the vegetation period through the early onset of spring phenophases [3][4][5][6][7] and later onset of autumn phenophases [8][9][10].The occurrence of drought associated with warming can affect production through a change in plant nutrient resorption in the following year, as well as shortening the vegetation period through earlier senescence [11].The early wood formation can be influenced by the length of the previous vegetation period due to the assimilates produced [12,13].As in the whole of Europe, Slovakia has experienced significant warming, the occurrence of long waves of heat and drought, and warmer winter temperatures [14][15][16] since the 1990s.Between 1871 and 2008, annual average air temperature was up by 1.1 • C and annual rainfall declined 5.6%, as well as there being snow cover in the whole area [17].Decreasing trends in precipitation in the period 1981-2013 were detected in December in the northern part of Slovakia, while the central and southern parts revealed increasing trends.Most of the stations showed increasing summer precipitation trends, especially in July [18].Forecasts by 2100 refer to the drying of southern regions, the growth of liquid precipitation, and the decrease in the number of days with an average freezing point at higher altitudes (800-1000 m a. s. l. [19].In the case of such significant climatic changes, it is possible to assume the risk of damage to vegetation by late frosts, but also the shift of the range of species to higher altitudes or higher vegetation stages with more favorable temperature and humidity conditions [20].Changing the reaction of woody plants to a warmer climate can also be monitored through a vertical phenological gradient that expresses a time shift in phenophases by one height, usually 100 m [21].With climate change and temperature rise at higher altitudes, the equilibrium of temperature differences and a decrease in vertical phenological gradients can be expected.One of the analyses that can capture the variability of phenophases is a descriptive phenological calendar.It is also possible to express the average onset and sequence of phenophases and to evaluate changes in these characteristics in space and time [22,23].The authors of phenological calendars capture the dynamics of vegetation on the territory at various scales [24][25][26][27][28].The use of the phenological calendar also affects human health.As a pollen calendar, it provides information on the flowering and reproductive capacity of allergenic plant species, as well as information on daily and seasonal concentrations of pollen in a given territory, thus preventing human health damage [29][30][31]. The aims of our work was determine the stability of the order of the phenophases, and to determine the vertical phenological gradient and trends in onset (presumably due to warming climate) of the native woody (Corylus avellana L.; Tilia cordata Mill.) and shrubs species (Crataegus oxyacantha L.; Prunus spinosa L.) at three stations in central and at two stations in south-western Slovakia from 1996-2015.

Study Site
In order to demonstrate the differences in the occurrence of phenophases and to determine the order of the phenophases at different elevations, we selected five phenological stations: Stupava (180 m), Zvolen (300 m), Dolná Súča (400 m), Černová (475 m) and Kysihýbel' (565 m) (Figure 1).The stations present different climate and location conditions.The environmental characteristics of the individual stations [21] are given in    July [18].Forecasts by 2100 refer to the drying of southern regions, the growth of liquid precipitation, and the decrease in the number of days with an average freezing point at higher altitudes (800-1000 m a. s. l. [19].In the case of such significant climatic changes, it is possible to assume the risk of damage to vegetation by late frosts, but also the shift of the range of species to higher altitudes or higher vegetation stages with more favorable temperature and humidity conditions [20].Changing the reaction of woody plants to a warmer climate can also be monitored through a vertical phenological gradient that expresses a time shift in phenophases by one height, usually 100 m [21].
With climate change and temperature rise at higher altitudes, the equilibrium of temperature differences and a decrease in vertical phenological gradients can be expected.One of the analyses that can capture the variability of phenophases is a descriptive phenological calendar.It is also possible to express the average onset and sequence of phenophases and to evaluate changes in these characteristics in space and time [22,23].The authors of phenological calendars capture the dynamics of vegetation on the territory at various scales [24][25][26][27][28].The use of the phenological calendar also affects human health.As a pollen calendar, it provides information on the flowering and reproductive capacity of allergenic plant species, as well as information on daily and seasonal concentrations of pollen in a given territory, thus preventing human health damage [29][30][31].
The aims of our work was determine the stability of the order of the phenophases, and to determine the vertical phenological gradient and trends in onset (presumably due to warming climate) of the native woody (Corylus avellana L.; Tilia cordata Mill.) and shrubs species (Crataegus oxyacantha L.; Prunus spinosa L.) at three stations in central and at two stations in south-western Slovakia from 1996-2015.

Study Site
In order to demonstrate the differences in the occurrence of phenophases and to determine the order of the phenophases at different elevations, we selected five phenological stations: Stupava (180 m), Zvolen (300 m), Dolná Súča (400 m), Černová (475 m) and Kysihýbeľ (565 m) (Figure 1).The stations present different climate and location conditions.The environmental characteristics of the individual stations [21] are given in Table 1.

Data
We used data from the database of the Climatological and Meteorological Information System of the Slovak Hydrometeorological Institute in Bratislava to study the phenological conditions in Slovakia.In order to capture the variability of vegetation during the year, we processed the phenophases of flowering BBCH scale 60, leaves unfolding-BBCH 11 and ripe of fruit-BBCH 86 [13].We focused on native species: C. avellana (european hazel-COA), C. oxyacantha (hawthorn-CO), P. spinosa L. (blackthorn-PS) and T. cordata (small-leaved lime-TC).The selection of monitoring areas and individual trees was carried out according to the followingprinciples: a locality corresponding to the character of the given area (slope, exposure), the number of observed samples was 10, the individuals were in good condition, and they were fertile and approximately the same age.Monitoring of phenophases was repeated three times a week.The observations were conducted between 1996 and 2015.From these data, we expressed shifts in the onset of phenophases indicating a change in climatic conditions.In the analysis, we expressed the average onset of phenophases (Ø) at stations in 180-565 m a. s. l.We also expressed the terms of the earliest (Min.) and later onset (Max.) over the period of 20 years.The difference between the least and the later onset of phenophases we have expressed as amplitude of the phenophases.Through the coefficient of variation (s x (%)) we identified the phenophases with the greatest and least interannual variability.The trend of onset of phenophases was calculated from linear regression as the slope of a regression line (day of the onset of phenophase against year).
In regard to the altitudinal zonation, we calculated the change in phenophase with altitude as vertical phenology gradient (days/100 m).It was calculated from linear regression as a slope of the regression line (altitude against the day of onset of phenophase).

Results and Discussion
One of the results of phenological observations are phenological calendars.In the locality or in its wider area, with similar climatic conditions, they express the order of the phenophases of the autochthonous woody species in the 20-year period.The phenological activity of the observed phenophases in the conditions of Slovakia begins with the flowering of the European hazel (BBCH 60 COA) and ends with the ripening of fruits of the small-leaved lime (BBCH 86 TC).Phenological calendars confirmed the stability of the order of the phenophases at all stations.The small change in the order can be considered insignificant in terms of a small time difference (1 day).We have found differences in the onset of phenophases between stations with altitude growth, when the onset of phenophases was delayed with altitude growth (Figures 2-6).The phenophases BBCH 60 was delayed with altitude for 49 days for the hazel, 16 days for the blackthorn, 10 days for the hawthorn, and 26 days for small-leaved lime.The phenophases BBCH 11 was delayed with altitude for the hazel for 20 days, 16 days for the blackthorn, 15 days for the hawthorn, and 9 days for the lime.The phenophases BBCH 86 were delayed with altitude by 16 days for the hazel, 15 days for the blackthorn, 13 days for hawthorn, and 26 days for lime.In several cases the phenophases onset of BBCH 60 and BBCH 11 was found earlier at the lower altitude (Černová) than at the higher altitude (Kysihýbel).The mean onset of phenophases was the same or only slightly different.We found that time shifts were not only due to an altitude effect, where delays in phenological phases are expected to increase.Phenophases BBCH 60 and BBCH 11 also were The phenophases BBCH 60 was delayed with altitude for 49 days for the hazel, 16 days for the blackthorn, 10 days for the hawthorn, and 26 days for small-leaved lime.The phenophases BBCH 11 was delayed with altitude for the hazel for 20 days, 16 days for the blackthorn, 15 days for the hawthorn, and 9 days for the lime.The phenophases BBCH 86 were delayed with altitude by 16 days for the hazel, 15 days for the blackthorn, 13 days for hawthorn, and 26 days for lime.In several cases the phenophases onset of BBCH 60 and BBCH 11 was found earlier at the lower altitude ( Černová) than at the higher altitude (Kysihýbel).The mean onset of phenophases was the same or only slightly different.We found that time shifts were not only due to an altitude effect, where delays in phenological phases are expected to increase.Phenophases BBCH 60 and BBCH 11 also were dependent on the other abiotic factor-exposures.At a higher altitude station (Kysihýbel-565 m a. s. l.), the earlier average onset (3-4 days) of the phenophase BBCH 60 and the same average onset of BBCH 11 due to south exposure and morphology was found, and the lower Černová station had plain morphology.In the period under review, the most pronounced phenological deviations of early (2014) and late onset (1997) of spring phenophases were observed at almost all phenological stations.These extremes were the response of trees to the development of the spring season.
Changes in the temperature and precipitation conditions of the environment due to the altitude can also be expressed using the vertical phenological gradient (VPG).This expresses the change of climatic elements in relation to the phenophases of the woody species in the boundaries of their vertical occurrence.It determines the difference in phenophase occurrence between the lowest and highest phenological stations, converted to 100 meters altitude [19].For the height interval of our stations (385 m a. s. l.) the VPG (Table 2) of BBCH 60 reached interval 3 (hawthorn)-6 (small-leaved lime) days/100 m, BBCH 11 2.4 (small-leaved lime)-4.9(European hazel), BBCH 86 2.7 (blackthorn)-5.1 (small-leaved lime) day/100 m height.The research [31][32][33] that dealt with the change of phenophases with altitude in Slovakia found the VPG of BBCH 60 TC is 4.1-4.7 days/100 m, BBCH 11 TC is 2.9-3 days/100 m, and BBCH 86 TC is 1.7 days/100 m.The research [34] found a delay of BBCH 60 PS 3 days/100 m and BBCH 11 PS 3.6 days/100 m.Similar results were obtained in beech forests [6].The research [35] showed that spring phenophases have advanced four weeks in Western and Central Europe, and have been delayed up to two weeks in Eastern Europe.The climate change over a longer period of time will also logically bring changes in the phenological characteristics of natural ecosystems.The magnitude of these changes is likely to depend on their stability and adaptation to new environmental conditions.One of the key indicators of change is also the trend analysis of phenophases.Climate change in the territory of Slovakia documents, according to our observations, for 20 years the early trend of the beginning of flowering (BBCH 60) of hazel, hawthorn and blackthorn at all stations by 4-12 days, which represents a shift of 0.2-0.6 days per year (Tables 3-7).  5.The characteristics of the phenophases in Dolná Súča (ø-average onset, σ-standard deviation, s x -variation coefficient [%], Min.-the earlier onset, Max.-the later onset, Amplitude = Max.− Min., Trend-the change in onset-days per year) and simple regression of the onset of the phenophases, p-value, correlation coefficient, p < 0.05; *-statistically significant correlation year against date) in 1996-2015.The earlier onset of spring phenophases due to climate change is valid for both Central Europe and Slovakia.From the results, we found that BBCH 60 COA started on average 7 days earlier than in 1964-1983 and 2 days earlier than 1994-2013 [36].The trend of an earlier flowering of the hazel by 0.7 days per year in Slovakia and the Czech Republic, as well as leaves unfolding by 1.8 days in the Czech Republic and 0.5 days in Slovakia, were found by researchers [37].Earlier flowering of the hazel by 0.24 days per year were also found in Poland [38] and 3.38 days per year in Germany, with a shift of 33 days from 2051-2080 [39].At three of the five stations, the trend of earlier BBCH 60 PS and BBCH 60 CO was statistically significant.The research [40] expects earlier onset of this phenophase by 20 days to the year 2100.As in our case, earlier flowering by 0.21 days per year was found in southern Moravia [41].The earlier development of trees can affect the number and size of early wood vessels due to the early spring temperature [42,43].The authors [13] observed damage after the sudden frost in May in some individuals of the Pedunculate oak, but they did not validate the hypothesis that the springtime ground frost had a negative effect on either tree-ring width or the number and size of earlywood vessels.The authors [44,45] said that species with late leaf development responded to climate change on average less than species with earlier leaf development.The BBCH 60 TC was started in the summer period, averaging from 6 June to 2 July at stable air temperature.The trend of this phenophase at Zvolen and Kysihýbel stations did not indicate any shift.At other stations, the trend changes were reflected in earlier and later shifts of 2 days without statistical significance.The statistically significant trend of earlier flowering of the small-leaved lime by about 2.8-4.4 days per year was found in Hungary [46].In the north, in the central part of European Russia, the shift in this phenophase was 0.03-0.13days per year [47].We recorded the average earliest onset of leaves unfolding (BBCH 11) of hawthorn and blackthorn on 8April at the lowest altitude station (Stupava 180 m).At the latest, the first leaves were unfolded of the small-leaved lime on the 3 May at the highest altitude station (Kysihýbel 565 m).Trend analyses showed, with the exception of the Stupava station, a shift of 2-14 days in most of the monitored species.The earlier development of small-leaved lime leaves was not statistically significant as in Lithuania, where authors reported the earlier onset of this phenophase 0.18 days per year [48].In our research were trends of a shift (12-14 days) of BBCH 60 PS to the earlier date that were statistically significant at most of the stations.The phenophase BBCH 86 began depending on the species and altitude of the phenological station.The trend analyses showed earlier onset of BBCH 86 of the hazel, hawthorn and blackthorn at most of the cases by 4-12 days without statistical significance.The exception was small-leaved lime, where we recorded an insignificant trend of later onset of 6-10 days (except at the Černová station).

Phenophase
The phenological response of tree species to the development and course of abiotic conditions, especially air temperature and rainfall, can also be evaluated using the variation coefficient (s x ).The highest variation coefficient was found for BBCH 60 COA (20.2-33.4%)regardless of the altitude, similar to other research [35,49].This indicates the unstable weather and temperature fluctuations in the early spring period.The equable course of onset of phenophases occurred at the end of April by decreasing the coefficients of variation.The flowering of the small-leaved lime (BBCH 60 TC), as a late flowering species, had the lowest variation coefficient (2.7-3.3%)compared to other early flowering species.Lower variability in the onset of late-flowering species was also found by researchers [50].Phenophases that occurred between the beginning of May and end of September had the lowest coefficients of variation (1.5-6.0%),likely because temperature conditions are stable and have the lowest variability during that period.For example, the variation coefficient of the BBCH 86 COA was 2.1-3.8%,which is comparable to the results from the Czech Republic (s x = 2%) and Slovakia (s x = 0.9%) [37].

Figure 1 .
Figure 1.The location of phenological stations.

Figure 1 .
Figure 1.The location of phenological stations.

Table 1 .
The environmental characteristics of the individual stations.

Table 1 .
The environmental characteristics of the individual stations.