Theor. Appl. Climatol.
81, 169176 (2005)
DOI 10.1007/s00704-004-0120-1
Department of Plant Biology and Agroenvironmental Biotechnology, University of Perugia, Italy
Olive flowering as an indicator of local climatic changes
F. Orlandi, L. Ruga, B. Romano, and M. Fornaciari
With 6 Figures
Received September 15, 2003; revised August 31, 2004; accepted October 10, 2004
Published online February 22, 2005 # Springer-Verlag 2005
Summary
In recent years many studies on climate change and its
impacts have been published. In this investigation the flow-
ering of the olive tree (Olea europaea L.) in central Italy
was related to climate and its usefulness as a bio-indicator
for climatic change has been studied.
An aerobiological method was used to determine the flow-
ering periods in each of 22 study years (19822003), and five
yearly target dates in correspondence to different flowering
phases were selected.
Climatic trends were studied through heat summations
(daily maximum, minimum and average temperatures) from
1 January to the annual day of full flowering; moreover
Growing Degree Days (GDD) and Chilling Units (CU) were
carried out since 1 January to 25 conventional dates in the
pre-flowering period.
Statistical analyses were carried out to study the relation-
ships among climatic trends (expressed by GDD and CU)
and the flowering phases. The principal result may be re-
presented by the close relationship between climate and re-
productive phenology to consider olive flowering as a good
indicator of climatic changes.
1. Introduction
Since the 1980s, climatic variations and global
warming trends and the consequent hydrological
changes have been studied by the scientific world
(IPCC, 1990, 1992).
Since 1900 the global and European annual
mean air temperatures have increased by 0.3
0.6
C (IPCC, 1998). Rambal and Hoff (1998)
have reported that during the last decades the
annual mean temperature of the Mediterranean
basin has increase more than the average glob-
al increase. Climatic variation is indicated by
changes in the mean values of the main weather
parameters, such as temperature and rainfall. In
addition, Mearns et al. (1997) noted that changes
in temperature and precipitation along with a
greater frequency of weather extremes (freezing,
drought, hail, etc.) have had serious effects on
agricultural yield. Since the phenological rhythm
of each species depends on seasonal meteorolog-
ical trends, climatic changes in the future may
cause changes in species distribution, as well as
time shifts in the onset of various phenophases
with probable consequences on crop productiv-
ity. In this way, phyto-phenology could provide
some indirect information about the principal
climate trends (Menzel and Fabian, 1999;
Chmielewski and Rotzer, 2001).
Recent studies indicate that the spring-time
temperatures in northern Europe have increased
during the last century. As a consequence, the
initiation of phenological phases such as leaf for-
mation and flowering have occurred earlier in
many species (Schwartz, 1999). In the last 50
years, the duration of the vegetative period has
increased by 13.3 days which is confirmed by an
earlier onset of the phenological phases in the
spring.
170 F. Orlandi et al.
In such studies several thermal parameters
(Growing Degree Days GDD, Growing Degree
Hours GDH and Chilling Units CU) are usu-
ally calculated as a function of seasonal trends
to explain the behaviour of the crop in relation-
ship to the climatic trends of the environment,
as well as to estimate the duration of the crop
cycle and predict the date when the crop will be
mature.
Using data from France, Spain, Portugal,
Algeria, Israel and Greece, Osborne et al.
(2000b) found that the flowering date in olive
is an indicator for climate warming. In this study
data from another a Mediterranean area, central
Italy, was used to check this phenomenon. Olives
can grow between the 30
45
latitudes in both
the northern and southern hemispheres, but are
found principally in the Mediterranean basin char-
acterized by warm and dry summers (Dallman,
1998). The Olive could therefore be used as a
bio-indicator for the whole Mediterranean
region.
In the Mediterranean basin, olive flowers
between April and June which is later than most
other tree species. This later date allows olive to
meet the requirements of an ample accumulation
of heat units during the growing season. Yearly
temperature variations control the timing of the
flowering period (Chuine et al., 1998).
Recent studies have used a pollen monitoring
methodology to record pollen release in olive, a
typical anemophilous species. The aerobiological
and phenological data were collected over a large
area (radius of about 50 km) in an attempt to
overcome the typical phenological problem of a
limited study area. The pollen quantities that
were monitored were used to interpret regional
variations in the reproductive phases in response
to the climate, while particular local events asso-
ciated with micro-climates were not considered.
Pollen monitoring of wild and cultivated species
may be used to correlate phenological phenom-
ena with climatic characteristics considering the
close relationship between the environmental fac-
tors and biological response (Osborne, 2000a,
2000b).
2. Materials and methods
A large area surrounding the city of Perugia
(central Italy) was monitored for 22 years
(19822003); olive pollen levels were analysed
using an aerobiological method described in ear-
lier works (Galan et al., 2001; Fornaciari et al.,
2002). The olive pollen was collected using a
pollen trap (VPPS 2000 Lanzoni model) made
up of two parts: a lower fixed part, and an upper
mobile one which has a small aperture through
which the airborne materials enter, by being
sucked in with a constant air flow volume
(10 l=min). The pollen content in the atmosphere
was observed and measured through microscopic
analyses, by determining the olive pollen grain
concentration per cubic metre of air. These data
were then expressed as hourly, daily or weekly
pollen concentrations.
In the literature, daily average pollen concen-
trations are used to determine the quantitative
standard parameters such as the pollen index
(Ip sum of the total pollen concentrations dur-
ing flowering) or critical flowering dates (first or
maximum pollen emission days).
In this study, the days on which the maximum
pollen concentrations were recorded (peaks of
pollen emission) and other flowering target
dates (expressed as the number of days from 1
January JD) were considered. These dates were
determined based on the partial summations of
the daily pollen concentrations. The partial pol-
len summations were considered as the 5, 10, 20,
50 and 70 percent levels of the total annual pol-
len count. The first two percentages (510) were
calculated to determine the dates of the initial
flowering phases in the olive groves, the next
two percentages (2050) were calculated to
determine the full flowering phase in olive, while
the last dates, associated with the 70% value of
the total yearly pollen emission, accounted for the
final flowering phases.
From a climatic point of view, the yearly heat
summations based on the daily thermal values
(maximum, minimum and average temperatures)
from 1 January until the annual maximum pollen
peaks (full flowering) were calculated in order to
determine the variations in the heat requirements,
in a given time series for, at a constant ontologi-
cal phase (flowering).
The commonly used climatic parameters,
GDD (McMaster and Wilhelm, 1997) and CU
were determined. These parameters were calcu-
lated daily from 1 January to 25 different dates
during the first six months of the year in an
 Olive flowering as an indicator of local climatic changes
attempt to objectively interpret the principal cli-
matic trends during the considered period. The
25 dates were chosen on the basis of 5-day inter-
vals from February 1 to June 1.
The GDD was calculated by
 
TMAX TMIN
GDD  T threshold;
2
with a threshold of 5
C:
The CU was calculated according to the
Utah method (Richardson et al., 1974). In this
method, a thermal range was chosen (39
C) in
which the maximum chilling value was recorded
if out of this temperature range, either higher and
lower, the chilling effect was reduced. The math-
ematical model uses hourly positive and negative
values to construct a curve which optimises the
chilling effect linked to weighed values re-
lated to each temperature. In accordance with the
mathematical model, the CU values were:
0 for T<1:4
C; 1 for T>19:5
C and
1 for T 5:2
C:
To study the effect of climate on olive flowering,
the best GDD and CU thresholds for full flowering
phase (70% pollen concentration) were first calcu-
lated, for all the years, using the Root Mean Square
Error (RMSE) statistical method. The time series
with the dates (JD) on which the thresholds were
achieved in each year were then plotted.
Correlation analyses were conducted among
the annual GDD-CU amounts calculated for the
171
25 different dates and the 5 flowering target dates
(in JD) in an attempt ascertain the relationships
between meteorological trends and plant behav-
iour. In addition a regression analysis was car-
ried out on the most significant meteorological
parameters considering the flowering target dates
as the dependent variable.
The meteorological data were obtained from
the weather station of the Central Ecological
Office in Perugia (Italy).
3. Results and discussion
The yearly heat summations calculated in corre-
spondence to the various peaks of pollen emission
are reported in Fig. 1. The annual heat require-
ments in olive are quite homogeneous, particularly
when average temperature is considered. These
results are of particular interest considering the
relationship between flowering dates and climate
changes. The flowering phenomenon in olive ap-
pears to be significantly related to constant heat re-
quirements expressed over in the whole time series.
The climatic factors recorded in this study are
expressed as the GDD and CU amounts (Fig. 2).
A warming trend can be noted in the marked
variations in the latter years. The CU amounts,
depicted in the upper graph show a clear decreas-
ing trend particularly from 1996. The lower CU
amounts are due to higher minimum temperature
values. During the same period, the GDD values
showed an increasing trend, although not as
marked as the preceding chilling phenomenon.
Fig. 1. Heat summations (
daily
minimum, maximum and average
temperatures) from 1 January to the
annual maximum pollen concentration
days
172 F. Orlandi et al.

Fig. 2. Thermal trends (GDD and CU) calcu-

lated from 1982 to 2003 for 25 days measured
every 5 days

The five flowering target dates based on the
various percentages of total pollen emission are
shown in Fig. 3. Three main sub-trends can be
observed which correspond to the periods
19821991, 19921995 and 19962003. In
the first interval, the JD which corresponded
to flowering occurred over a large range and
showed a constant trend. In the two other
periods, the target dates gave a steeper slope
with an earlier flowering in the final years.
 Olive flowering as an indicator of local climatic changes 173

Fig. 3. Dates of different flowering percentage targets from 1982 to 2003

Fig. 4. CU and GDD values until 1

June in the study period with trend
lines

These results support the hypothesis that dur-
ing the last decade, particular phenological
trends appeared which were probably linked
to climatic variations.
The time trends of the GDD-CU values calcu-
lated from 1 January until 1 June (average date of
the local olive flowering) are shown in Fig. 4. The
climatic trend is evident in both the GDD and CU
values. The CU values are listed in decreasing
order, while the GDD values show an increasing
trend. By introducing polynomial trend lines into
the CU and GDD values, the thermal components
in the chilling and heat effects become evi-
dent. In Fig. 3, the steeper slope of the sub-trend
for the period from 19962003, may be princi-
pally related to the thermal chilling effect
(variations of the chilling units).
The average CU and GDD values are reported
for the three principal periods shown in Fig. 4
along with the percentage differences among them.
From 1982 to 1991, the average CU and GDD
amounts were 1168 and 1359, respectively while
174
in the second period (19921996) they were
1002 and 1436, respectively with a 14% decrease
in the CU values and a 5% increase in the GDD
values. In the third period (19972003), the aver-
age CU amounts decreased 24% (759) in com-
Fig. 6. Regression analysis between last flowering percentage target (>70%) and CU from Jan 1 to 1 June as independent
variable
F. Orlandi et al.
parison to the second period, while the average
GDD values increased 8% (1555).
The effect of climate on olive flowering was
carried out on the best GDD (1434) and CU
(996) values for full flowering over all the years
Fig. 5. Calendar dates on which the
best GDD and CU thresholds for full
flowering were recorded for each
year
 Olive flowering as an indicator of local climatic changes
and permitted to plot the time series (JD) on
which the threshold values were determined
(Fig. 5). The figure shows as both CU and
GDD threshold values are realized earlier in the
last years in accordance with the phenomenon
interpreted by the flowering dates.
Statistically the highest correlation value
(r>0.8) was observed among the five flowering
target dates and the thermal amounts (GDD and
CU) when the final thermal amounts (1 June) and
the flowering target dates were considered. These
results indicate that the flowering phenomena are
dependent on the thermal trends, in particular the
highest correlations were obtained when the ther-
mal amounts were calculated using a final date of
summation after May.
The regression analysis which used the last
flowering target date (>70%) as the dependent
variable and the annual CU amounts calculated
on 1 June as the independent variable (the most
frequently correlated climatic parameters) dem-
onstrated that the plant behaviour could be in-
terpreted well by calculating the chilling units
(Fig. 6). In this analysis, the independent climatic
variable (CU 1 June) was highly significant.
Moreover, the residuals of the regression reached
the 5-day value but most of these were grouped
in the 2-day range. In this way the CU values
could be used to determine, with an average error
of 2 days, the date when the highest olive pollen
concentrations (70%) were recorded.
4. Conclusions
The results of this study indicate that there is a
close relationship between climate and reproduc-
tive phenology in olive. The relationships among
all the flowering target dates and the thermal
amounts (CU and GDD) indicate that olive flow-
ering can be considered a good indicator of
climate changes. This relationship is marked by
the notable stability between the biological
responses and the annual thermal amounts in
olive. Consequently olive can be used to interpret
climate variations.
All of the different flowering target dates had
high correlation values with climate variables
(GDD-CU amounts) which indicates that the
same thermal effects may also be noted in all
the sub-phases of the flowering process (initial-
full-final flowering).
175
In the study area, after May the physiological
response of the plant (formation of tetrad pollen
and bi-nucleate pollen) become very sensitive to
small increments in heat amounts because the
heat demand for flowering is nearly fulfilled.
Some researchers (Moonen et al., 2001) con-
firmed that in relation to the climate, the changes
are mainly due to an increase in the minimum
temperatures rather than to changes in the max-
imum temperatures. The climatic and phenologi-
cal trend from 1996, in the study area, was
characterized by lower chilling unit values.
The influence of chilling in olive as a highly
demonstrated dormancy regulator and the capac-
ity of the chilling unit formula used (Utah model)
to interpret both chilling effect and chilling
negation (heat amount) explain the significant
results of CU applied to the olive species.
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Authors address: F. Orlandi (e-mail: fabor@unipg.it),
L. Ruga, B. Romano and M. Fornaciari, Department of Plant
Biology and Agroenvironmental Biotechnology, University
of Perugia, Borgo XX Giugno 74-06121 Perugia, Italy.