417

Adv. Hort. Sci., 2019 33(3): 417-431                                                                                                    DOI: 10.13128/ahs-24618 

Climate change effect on the bud break 

and flowering dates of the apple trees 

in mountainous and plain regions of 

Algeria 
 
 
A. Abed 1, 2 (*), M. Bonhomme 3, A. Lacointe 3, G. Bourgeois 4, D. Baali-

Cherif 1 
1       National School of Agronomic Sciences, Algiers, Algeria. 
2       Laboratory Water‐ Rock ‐Plant, Khemis‐Miliana University, Algeria. 
3       Clermont Auvergne University, INRA, PIAF, F‐63000 Clermont‐Ferrand, 

France. 
4     Agriculture and Agri‐Food Canada, Saint‐Jean‐sur‐Richelieu Research 

and Development Centre, Saint‐Jean‐sur‐Richelieu (QC), Canada. 
 
 
Key words: budburst, flowering, Golden delicious, modelling, temperature. 

 
 
Abstract: Global warming is a strongly felt reality in recent years in Algeria. The 

fruit trees crop is particularly exposed to the impact of this warming, especially 

apple trees. A comparative study has been realized between a chronological 

daily temperature series from 1980 to 2016, and phenological data series (bud-

burst and flowering) from 2000 to 2016, regarding the apple tree variety of 

Golden Delicious in two zones of Northern Algeria, Sidi Lakhdar (town of Ain 

Defla, in an altitude of 211 m) and Benchicao (town of Médéa, in an altitude of 

1133 m). Some contrasting tendencies according to sites and periods have been 

demonstrated: very significant warming at Sidi Lakhdar site in autumn and 

spring, in particular in October and April, disturbing thus the entrance of the 

buds in the endodormancy and ecodormancy. The result is a late action of the 

cold until February, which proved to be insufficient. However, no average 

warming has been demonstrated at the Benchicao site, where the tempera-

tures between November and January were cold enough to satisfy the need of 

cold units and raise the endodormancy. It seems that the failure to fulfill the 

need of cold units at Sidi Lakhdar site has strongly affected the goodness of fit 

of the classic phenological models, confirming indirectly the existence of more 

complex physiological processes (not taken in consideration by models), which 

manifest themselves in limited zones such as Sidi Lakhdar site. 

 
 

1. Introduction 

 
     According to the experts of the Intergovernmental Group of the 
Climate Evolution (IGCE), from now on to the end of the 21st century, the 
average temperature will be raising from 2 to 6°C in Europe following the 
regions, the climatic models and the socio-economic scenario. The sum-
mer droughts will be more intense as well (Giannakopoulos et al., 2005; 

(*)
 

Corresponding author:  
abedlila24@yahoo.fr 
 
 
Citation: 
ABED A., BONHOMME M., LACOINTE A., BOUR-
GEOIS G., BAALI-CHERIF D., 2019 - Climate chan‐
ge effect on the bud break and flowering dates of 
the apple trees in mountainous and plain regions 
of Algeria. - Adv. Hort. Sci., 33(3): 417-431 
 
 
Copyright: 
© 2019 Abed A., Bonhomme M., Lacointe A., 
Bourgeois G., Baali-Cherif D. This is an open 
access, peer reviewed article published by 
Firenze University Press 
(http://www.fupress.net/index.php/ahs/) and 
distributed under the terms of the Creative 
Commons Attribution License, which permits 
unrestricted use, distribution, and reproduction 
in any medium, provided the original author and 
source are credited. 
 
 
Data Availability Statement: 
All relevant data are within the paper and its 
Supporting Information files. 
 
 
Competing Interests:  
The authors declare no competing interests. 
 
 
 
Received for publication 15 January 2019 
Accepted for publication 3 September 2019

AHS 
Advances in Horticultural Science

http://creativecommons.org/licenses/by/4.0/
http://creativecommons.org/licenses/by/4.0/
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Adv. Hort. Sci., 2019 33(3): 417-431

418

Gleizer et al., 2007). 
     According to Legave (2009), a worrying accelera-
tion of the global warming has appeared during the 
1990 decade and much more during 2000 decade. In 
occidental Europe and the Mediterranean Basin, on a 
recent period of 30 years (1973-2002), we can esti-
mate the average increase of the annual tempera-
ture at about 1°C since the end of 1980’s. Regional 
differences are noticed though, with a warming rela-
tively marked in the region of Meknes in Morocco 
(2.3°C) (Balaghi, 2017), definitely higher than the one 
marked in the South-West of France (+1.3°C in 
Nimes)(Legave, 2009). 
     The global warming will affect, and has already 
notably done, a wide range of physical/biological sys-
tems and human activity sectors, among which agri-
culture (including livestock) and its principal function 
of producing and nutrition (Seguin, 2010). For 
Algeria, the 21st century shall be characterized by 
temperatures increase, in the order of 1.0 to 1.5°C at 
the horizon of 2020 (Fourth report of the IGCE in 
Bourchef, 2013) and precipitations decrease in the 
order of 15 to 20%. Extreme climatic phenomena are 
already affecting the region, like the rain and thun-
derstorms of November 2001 in Algiers and October 
2008 in Ghardaia, and the cold waves in January 2005 
and February 2001 in all Algeria. All these events can 
be qualified as historic at least regionally. Some simu-
lations realized for two types of agricultural years in 
terms of pluviometry (normal and dry), show at the 
horizon of 2020 a decrease in the yield of winter 
cereals from 6% to 14% according to the geographi-
cal regions and the year type in Algeria (Tabet-Aoul, 
2000; Tabet-Aoul and Bessaoud, 2009). 
     Phenology is the study of the occurrence of peri-
odic events in animal and plant life in relation with 
the climate variations. Those are characters that 
interpret the organisms’ adaptation to the climatic 
variation (Chuine, 2005). The task of plant-phenology 
is to observe and record the periodically recurring 
growth stages. Leaf unfolding, flowering of plants in 
spring, fruit ripening, colour changing and leaf fall in 
autumn  are all examples of phenological events 
(Koch et al., 2006). 
     It has been designated as a key point to evaluate 
the global warming impact on the agricultural cultiva-
tions (Moriondo and Bindi, 2008). Many studies have 
pointed an agreement which many species advanced 
the spring phenology events (budburst and blooming 
dates) particularly (Doi and Katano, 2008; Gordo and 
Sanz, 2010; Malagi, 2014). Since distinct phenological 
stages were defined decades ago (Baggiolini, 1952; 

Lichou et al., 1990; Meier et al., 1994), a comparison 
of available definitions of phenological stages in cher-
ry used independently throughout Europe showed 
overlaps and shortcomings; hence, harmonisation 
was reached in this respect in the COST Cherry FA 
1104 working group 2 (cherry phenology and climate 
change) based largely on the acceptance of the BBCH 
scale and agreed standard cultivars for phenology 
monitoring. Cultivars were selected on the basis of 
early, medium and late flowering and most widely 
grown throughout Europe. This contribution presents 
the agreed phenology stages in both visual and word-
ing evidence. Similarly, this contribution presents the 
agreed cultivars to be monitored in future for phe-
nology and climate change effects for harmonization 
(Wenden et al., 2017). 
     In this context, the fruit arboriculture seems rela-
tively vulnerable from the fact of some of its charac-
teristics, rather biological (eg: the fruit trees sustain-
ability and their need to many years of growth before 
fruiting) than economic. Compared to other produc-
tions (annual cultivations), the fruit arboriculture is 
particularly exposed to unfavorable climatic impacts 
from the fact of multiannual consequences (alterna-
tion of production after ceasing) and accumulative 
(repeated impacts on the tree architecture). On the 
socio-economic level, strong links have been woven 
during the time between the product and its produc-
tion place (eg: Provence almonds, Roussillon apri-
cots…etc). This characteristic developed in France, 
for commercial valorization reasons, in a regulatory 
form of origin and quality naming (eg: Agen prunes, 
Lorraine plums…etc.). From this fact, the substitution 
of varieties and much more species for long-term cli-
matic adaptation reasons seems relatively difficult to 
be implemented, probably risking to encounter regu-
latory and human obstacles (Legave, 2009). 
     These characteristics constitute an obstacle to the 
fast changes, not only to the variety range but also to 
the cultivation systems to cope with rising tempera-
tures or other constraints from climate change. This 
climate vulnerability has already been expressed in 
t h e  2 0 0 0 s  b y  s t r o n g  p r o d u c ti o n  i r r e g u l a r i ti e s . 
Unprecedented accumulations of unfavorable climat-
ic conditions (frost, high temperatures, excessive 
rainfall) have been observed during key phases of the 
annual cycle of trees, from flowering to fruiting. 
Thus, in southern France, very significant production 
losses were provoked, especially in 2007 for cherry 
trees following stormy episodes in May and June, 
which strongly penalized the French production, and 
in 2008 for apricot following episodes of excessive 



Abed et al. ‐ Climate change effect in apple flowering

419

heat as blooming approached. Sensitive varieties 
have had abortion rates that strongly penalize the 
national production. 
     Phenological notes on flower buds of fruit trees, 
collected under contrasting temperature (time and 
place) conditions in Europe, showed a significant 
advance of the different phenological stages, espe-
cially the flowering dates, for all the places. Modeling 
work on spring phenology strongly suggests that 
warming has two opposite effects: (1) in autumn and 
early winter, a slowdown in the satisfaction of cold 
unit needs, delaying endodormancy; (2) at the end of 
winter and in spring, an acceleration of the satisfac-
tion of the heat needs during the ecodormancy 
phase. The more pronounced intensity of this latter 
effect, consistent with the more pronounced increas-
es in temperature at the end of winter-early spring 
than in autumn, largely explains the advances in 
flowering (Legave et al., 2009). 
     The analysis of flowering dates over long periods 
in Western Europe for the Golden Delicious apple 
variety reveals more significant progress in the North 
of the continent (10 days) than in the oceanic west 
(6-7 days) and a shortening of flowering time in con-
tinental regions (Legave et al., 2012). These regional 
differences across Western Europe led to a decrease 
in spatial variability, that is to say, smaller differences 
between the flowering dates in the contrasting 
regions (decrease of 8-10 days for complete flower-
ing between the Mediterranean and continental 
regions). Modeling studies, based in particular on the 
correlations between the average temperature of the 
period of ecodormancy and the observed flowering 
dates, confirm the notion that flowering advances 
and shortenings are mainly due to a faster satisfac-
tion of the demand for heat units (Legave et al., 
2015). 
     However, delayed endodormancy has also been 
noted in the oceanic and Mediterranean regions, 
which may explain the shorter advances in these 
areas despite similar or greater warming and ulti-
mately lead to delayed flowering. The joint statistical 
analysis of flowering date series for the Golden 
Delicious variety and temperature dynamics reveals a 
geographical diversity of responses to warming from 
autumn to spring. Temperate climates in Europe are 
characterized by flowering progress, while soft cli-
mates are characterized by flowering progress or sta-
tionary flowering dates (eg. Morocco and Brazil), 
(Legave et al., 2015). At the same time, Legave et al. 
(2015) and El Yaacoubi et al. (2016) have shown in 
mild winter conditions, a longer flowering time asso-

ciated with the high average temperature of the 
endodormancy period. 
     In the same context, a comparison of dormancy 
dynamics of vegetative and floral buds of apple and 
almond trees was recently conducted between 
southern France, southern Brazil, and northern 
Morocco. Differences in dormancy intensity and 
kinetics have been identified in relation to regional 
differences in the satisfaction of cold needs and dif-
ferent levels of requirements of the genotypes stud-
ied. The observed diversity of dormancy patterns 
suggests that genotypes adapted to mild climates 
(eg, almond trees, apple trees with low cold needs) 
are characterized by the ability of vegetative buds to 
remain in a state of low dormancy and ability of 
flower blanks to grow rapidly, guaranteeing the 
absence of phenological anomalies subsequent to 
foliage and flowering (El Yaacoubi et al., 2015). 
     The apple tree is currently an important fruit 
species in Algeria. Production is the most important 
fruit production, but it does not sufficiently cover the 
demand. The central region (Medea - Blida - Ain 
Defla) totals about 7400 ha or about a quarter of the 
total area. Apple cultivation has grown considerably, 
from 30,000 ha in 2003 to 41,000 ha in 2013, with a 
production reaching 400,000 tons (F.A.O 2013, men-
tioned by Meradi, 2015). Due to the levels of yield 
and quality obtained, the Golden Delicious variety is 
one of the three varieties that dominate the Algerian 
market, particularly in the region of Medea (Golden 
Delicious 70%, Starkrimson 20% and Granny Smith 
5%) (Hadj Sahraoui, 2014). The apple “hanna”, of its 
real name “anna”, is a new variety of apple trees 
introduced in Algeria. It is planted in less cold areas, 
in the center of Algeria on the perimeter of high chel-
lif in Ain Defla, in the west on the Sebaou valley of 
Telemcen and in the east to Khenchela and M’sila. 
They are among the varieties less demanding in cold 
and generally give apples of lesser quality, hardly 
storable (Hamdani et al., 2016). 
     However, apart from regionalized studies aimed 
at predicting climate change through time series of 
temperature and rainfall and estimating its impact on 
crops through the increase of yields in all regions of 
Algeria including Constantine region in the east of 
the country (Kherief Nacereddine and Alatou, 2004; 
Tabet, 2008; Zekri et al., 2009) and Oran region in the 
west (Benabadji and Bouazza, 2000; Labani et al., 
2006), no study on phenological development as a 
key element to characterize the impact of climate 
change has been undertaken. We therefore wanted 
to begin to fill this gap with this study aiming at first, 



Adv. Hort. Sci., 2019 33(3): 417-431

420

the characterization of climate change via tempera-
ture series and the search for a possible impact on 
the phenology of the apple tree and, in a second 
step, the determination of the critical periods with 
regard to the accumulation of cold units and units of 
heat, by the implementation of the classical pheno-
logical models. For this, we analyzed the time series 
of phenological data of the Golden Delicious variety 
in two contrasting zones from the climatic point of 
view: a zone of plain with a rather warm climate, Sidi 
Lakhdar (town of Ain Defla) and a cooler zone in alti-
tude, Benchicao (town of Medea). 
 
 

2. Materials and Methods 

 

Sites and climatic data 

     The temperature data recorded for each site are 
shown in Table 1. The two zones selected in this 
study are: Sidi Lakhdar (town of Ain Defla, latitude: 
36° 15 ‘50’’ N, longitude: 2° 09’ 39’’ E, altitude 211 m, 
located in the center of Algeria 145 km south-west of 
Algiers) known for its semi-arid climate with a mild 
winter and a very hot summer, and Benchicao (town 
of Médea, latitude: 36° 11 ‘59’’ N, longitude: 2° 50’ 
55’’ E, altitude 1133 m, located 80 km south-west of 
Algiers) in a mountainous area with a warm temper-
ate climate. 
     Daily maximum and minimum temperature data 
obtained over a period of 37 years (1980 to 2016) 
were collected at weather stations near selected sites 
belonging to the National Office of meteorology. 
Average temperatures were calculated using maxi-
mum and minimum temperatures. Missing daily data 
were estimated using two methods: 
     A linear interpolation for some values over 1 to 3 
days (means to fill the missing values of Tmax and 
Tmin were carried out): Correlations with another 

site for the longest periods namely; between the sta-
tion of Sidi Lakhdar and the station of Chlef (latitude 
36° 10’ N, longitude 1° 20’ E, altitude 116 m) for the 
month of May of the year 2005, and between the 
station of Benchicao (Médéa) and the station of 
Bordj Bou Arreridj (latitude 36° 04 ‘23’’ N, longitude 
4° 45’ 39’’ E, altitude 930 m) for the months of 
January, February, March and April of the year 1980 
and the month of May of the year 2001. 
     Similarly, a correlation was made between the 
Médéa site and the Sétif meteorological station (lati-
tude 36° 11 ‘28’’ N, longitude 5° 24’ 49’’ E, altitude 
1038 m) for the months of September, October and 
November of the year 1981, and February and 
December of the year 1990. 

Phenological data 
     Data collected from 2000 to 2012 were provided 
by specialized state agencies. These are average 
dates that represent all the orchards visited. Those 
from 2013 to 2016 were collected directly from the 
same orchards, which were among the most apple 
orchards planted at both sites. Phenological monitor-
ing 3 to 4 times a week was carried out on adult 
trees, the number of which sufficiently covered the 
total area of a given orchard (50%), respecting the 
two orientations (North-South and West-East). These 
orchards have not undergone any chemical treat-
ment to break endodormancy or accelerate flower-
ing. Phenological stages were described according to 
the BBCH scale (Meier et al., 1997, 2001). The pheno-
logical stages of bud break (bud burst, Baggiolini 
stage C and stage 51 of the BBCH scale) and early 
flowering (10% open flowers, Baggiolini F1 stage and 
61 BBCH scale) were observed from 2000 to 2016 on 
the two apple orchards maintained according to con-
ventional horticultural practices. Both stages were 
reported affected when 60% of the trees in the 
orchard had reached the given stage. 

Table 1 - Phenological and temperature data collected in climate-contrasting sites for ‘Golden delicious’ apple trees

Site Benchicao (MD) Sidi Lakhdar (SD)

Region (town) Medea Ain Defla

Latitude/longitude  36°11' 59'' N / 2°50' 55'' E 36°15' 50'' N / 2°09' 39'' E

Altitude (m) 1133 211

Climatic area sub-humid semi-arid

Period recorded  of temperature 1980-2016 1980-2016

Bud burst stage and observation period a BBCH 51 / 2000-2016 BBCH 51 /2000-2016
Flowering stage and observation period a BBCH 61 / 2000-2016 BBCH 61 /2000-2016

a: BBCH 51, 61; stages in phenological code BBCH (Meier, 1997), are respectively swelling buds of inflorescences and 10% of flowers 
open.



Abed et al. ‐ Climate change effect in apple flowering

421

A, B and C. The parameter A determines the width of 
the window on which the function is not zero. The 
larger the value, the larger the temperature range 
over which the cold units are wide. Parameter B 
determines the sharpness of the response curve and 
its asymmetry. The more B differs from zero, the 
s h a r p e r  t h e  i m a g e  ( a n d  m o r e  a s y m m e t r i c ) . 
Parameter C determines the value of the average 
response when B is close to zero and represents a 
limit to the temperature range over which cold units 
accumulate, when B is significantly different from 
zero. 
     The Wang model was first defined by Wang and 
Engel (1998). It is characterized by an optimum and is 
not symmetrical. This concerns the family of the beta 
function. It is composed of three parameters, namely 
Tmin, Topt and Tmax (minimum, optimal and maxi-
mum temperatures). 
     The Sigmoid model was introduced by Hänninen 
(1990). It consists of two parameters, D and E. The D 
parameter defines the sharpness of the response. 
Values far from zero induce a sharper response 
curve. The parameter E is the average response tem-
perature. 

Smooth Utah/ Wang and Smooth Utah/ Sigmoid 
     T h e  S m o o t h  U t a h  m o d e l  w a s  i n t r o d u c e d  b y 
Bonhomme et al. (2010) and is a smoothed version of 
the Utah function proposed by Richardson et al. 
(1974). This function assumes that cooling can occur 
only over a range of temperatures and has four para-
meters: Tm1, Topt, Tn2 and min. Negative cooling 
values can be accumulated on hot days, increasing 
the amount of cold to reach. 
     Tm1: This parameter defines the sharpness of the 
decrease of the cold effect on the endodormancy of 
the buds. The lower Tm1, the slower is the decrease. 
     Topt: This parameter corresponds to the optimum 
average daily temperature, for which a cooling unit is 
accumulated each day. 
     Tn2: This parameter defines the intermediate 
response, i.e. the temperature (above Topt) that has 
half of Topt’s effectiveness for inducing endodorman-
cy. 
     M i n :  T h i s  p a r a m e t e r  d e fi n e s  h o w  m u c h  t h e 
impact of high temperatures can be negative. 
When min = 0, high temperatures do not have a neg-
ative impact on endodormancy release. When min = -
1, the negative impact of a day that is too hot is 
equivalent to the positive effect of a day in Topt. 
     Each model is characterized by efficiency (EFF), an 
estimated time (t0) and a quadratic error (RMSE: 
Root mean square error). 

Modeling and data analyses 
     To better explain the phenological behavior of the 
Golden Delicious variety in the two sites studied and 
to highlight the effect of the temperatures on the lat-
ter in terms of satisfaction in cold units and heat 
units, statistical analyses were carried out under R (R 
Development Core Team 2008), concerning regres-
sion curves between the different temperature com-
ponents (minimum, average and maximum) and the 
year as well as the two phenological stages (bud 
burst and flowering). Similarly, parametric name cor-
relation tests of Spearman were performed between 
two variables namely annual and monthly tempera-
ture (minimum, average and maximum) and year on 
the one hand and phenological stages on the other 
hand. Calculation and establishment of cold unit 
accumulation curves were performed using the Utah 
model (Richardson et al., 1974). 

Utah model 
     The Utah model was designed by Richardson et al. 
(1974). This model combines the cold units for tem-
peratures between 0 and 16°C and associates a nega-
tive value with temperatures higher than 16°C. This 
model is built to use fixed degree-days (independent 
of cold units) to predict bud break. The Utah model 
(Richardson et al., 1974) transforms the hourly tem-
perature into a cold unit from -1 to 1. The cumulative 
number of Utah cold units at time t is expressed as 
follows: 

UCUtot =  

     With (U= 0 for T≤1.4°C, U= 0.5 for 1.4°C <T≤2.4°C, 
U= 1 for 2.4°C <T≤9.1°C, U= 0.5 for 9.1°C <T≤ 12.4°C, 
U= 1 for 12.4°C <T≤15.9°C, U = -0.5 for 15.9°C 
<T≤18.0°C, U = -1 for T≥18.0°C) (Ricard, 2014). 

Phenological modeling platform PMP5.5 
     The phenological models were adjusted using the 
Phenology Modeling Platform (PMP5.5) proposed by 
Chuine et al. (2013). PMP5.5 is an environmental-use 
interface aimed solely at managing the construction 
of a phenological model, fitting a phenological model 
to the data and simulating using a phenological 
model. The best results of the bud burst and flower-
ing date prediction in the two studied sites are 
obtained by two-phase models (knowing that phase 
1 corresponds to the accumulation of cold units and 
phase 2 corresponds to the accumulation of heat 
units ) quoted below. 

Chuine/Wang and Chuine/Sigmoid 
     The Chuine model has been described in Chuine 
(2000) and is composed of three parameters, namely 

Tu

t

1





422

Adv. Hort. Sci., 2019 33(3): 417-431

3. Results 
 
General climatology. Annual tendencies 
     The annual average maximum, medium, and mini-
mum temperatures for both sites are shown in figure 
1. The linear regression of mean annual tempera-
tures over the 36 available years revealed a signifi-
cant warming (P = 0.004) at the Sidi Lakhdar (SD) site, 
with a significant increase in the mean annual mini-
mum temperatures (P = 0.001), and less for the aver-
age annual maximum temperatures (P = 0.04). There 
is rather a cooling tendency at mountain site of 
Benchicao, although not significant (P = 0.09), con-
cerning the annual average and where the maximum 
temperatures experienced some significant regres-
sion (P = 0.001). The hottest years were 1990, 2010 
and 2007 at the site of Sidi Lakhdar and 2016, 1997 
and 2000 at Benchicao site. 

Tendencies for the autumn‐spring period 
     A seasonal analysis from the 36 years available 
shows marked differences between the two sites. 
The monthly average temperature tendencies for the 
months of October to May (minimum, mean and 
maximum daily temperatures) measured during the 
period 1980 to 2016 for the two sites (Sidi Lakhdar 
and Benchicao) are summarized in Table 2 and figure 

Table 2 - Temperature data collected characteristics in the two studied sites in Algeria during 36 years

* p<0.05, ** p<0.01.

Fig. 1 - Average annual temperatures (minimum, average, maximum) for 
the two sites, Sidi Lakhdar (SD) and Benchicao (MD) from 1980 to 
2016. *, ** indicate the significance level of the correlation for P 
<0.05 and for P <0.01, respectively. Sidi Lakhdar: (SD) Tmin: y = 
0.0403x - 66.906 (R² = 0.33**), Taverage : y = 0.0305x - 41.183 (R² = 
0.21**), Tmax: y = 0.0234x - 21.077 (R² = 0.0864). Médéa:(MD) 
Tmin: y= 0.0122x - 12.479 (R² = 0.03), Taverage: y = -0.019x + 
54.187 (R² = 0.090), Tmax: y = -0.0503x + 121.02 (R² = 0.31**).

Month Daily temperature

Mean daily temperature during 36 
years in °C

Correlation coefficient of trends and level of significance

Sidi Lakhdar Benchicao
Sidi Lakhdar (SD) Benchicao (MD)
R p R p

October Average 21.3 17.4 0.40 0.01* 0.07 0.50

Maximum 27.0 21.6 0.38 0.018* 0.14 0.40

Minimum 15.6 13.3 0.44 0.006** 0.36 0.028*
November Average 15.7 11.4 -0.004 0.1 - 0.40 0.007**

Maximum 20.3 14.7 - 0.03 0.842 0.20 0.008**

Minimum 10.8 8.1 0.11 0.48 - 0.17 0.30
December Average 12.0 8.0 0.17 0.28 - 0.16 0.16

Maximum 16.4 10.9 0.10 0.556 - 0. 17 0.31

minimum 7.6 5.2 0.19 0.26 0.009 0.966
January Average 10.9 7.3 0.35 0.03* - 0.20 0.08

Maximum 15.3 10.2 0.24 0.143 -0.20 0.23

minimum 6.4 4.6 0.32 0.051 0.10 0.54
February Average 11.9 8.1 0.11 0.48 -0.32 0.005**

Maximum 16.8 11.2 0.047 0.783 -0.47 0.003**

Minimum 6.8 5.0 0.16 0.34 - 0.22 0.18
March Average 14.2 10.5 0.01 0.51 -0.23 0.03*

Maximum 20.0 14.3 0.008 0.961 -0.47 0.030*

Minimum 8.5 6.8 0.25 0.13 - 0.025 0.88
April Average 16.6 13.3 0.42 0.008** -0.07 0.51

Maximum 23.0 17.5 0.36 0.027* 0.012 0.565

Minimum 10.4 9.03 0.49 0.002** 0.18 0.28
May Average 21.0 17.9 0.32 0.04* -0.1 0.38

Maximum 27.9 22.7 0.21 0.19 0.027 0.403

Minimum 14.3 13.0 0.40 0.012* 0.089 0.600



Abed et al. ‐ Climate change effect in apple flowering

423

2. Table 2 generates Spearman parametric name cor-
relation values between maximum, average and min-
imum monthly temperatures and year, and where p 
is the level of significance and R is the correlation 
coefficient. 
     We focused on the period from October to May, 
which is the period that most affects the physiological 
processes associated with the spring phenology of 
flower buds of fruit trees in our region. Average 
October temperatures are high and increase signifi-
cantly at Sidi Lakhdar site. The month of April is also 
warming significantly on this site (Table 2, Fig. 2). No 
significant tendency is recorded for the other months. 
Correlations on monthly temperature tendencies also 
clearly showed significant summer warming in July at 
Sidi Lakhdar site (data not shown). At mountain site of  
Benchicao, on the other hand, as already indicated 
above, during the 36 years, no significant warming is 
recorded in average temperature. On the contrary, 
average temperatures decreased in November and 
February (P = 0.007 ** and P = 0.005 *, respectively). 
      Regarding average minimum temperatures, the 
lowest values were recorded during the month of 
January for both sites with 6.4 and 4.6°C. The highest 

minimum temperature value of 12.1°C and the lowest 
value of 8.2°C were recorded by order in 2006 and 
1991 at the site of Sidi Lakhdar for this month of 
January. At mountain site Benchicao, the highest value 
of 9.7°C is reported in 2000 compared to a lower value 
of 6.6°C in 1980. The site of Sidi Lakhdar experienced 
extreme maximum temperatures during the months of 
October and April which explains the significance of the 
increase in average temperatures during these two 
months (Fig. 2a). Significant regressions of maximum 
temperatures were recorded at the Benchicao site dur-
ing the months of November, February and March. 

Phenological development 
     Comparisons of the phenological tendencies of 
the apple tree (in terms of bud burst and flowering) 
in the two contrasting environments were made 
from the 16 years available. For budding dates of 
flower buds at Sidi Lakhdar site, some variation 
between years was revealed with marked tardiness 
during the years 2002, 2007, 2012, 2013 and 2016, 
when there was a bud break between the end of 
March and the first days of April and an early fruit 
maturity in 2000, 2003 and 2006, but the overall ten-
dency for all years is not significant (P = 0.07). The 
tendency towards the advancement of flowering 
dates (Fig. 3) is also not significant (P = 0.24), the ear-

Fig. 2 -  Evolution of average monthly temperatures, on both sites, for 
months where the trend is significant at Sidi Lakhdar (October 
and April) and at Benchicao (November and February). *, ** 
indicate the significance level of the correlation for P <0.05 and 
for P <0.01, respectively. Sidi Lakhdar: (SD) Average April: y = 
0.068x - 119.18 (R² = 0.2252**), Average October: y = 0.0742x - 
126.9 (R² = 0.1909**). Médéa:(MD) Average February: y = -
0,0799x + 167,72 (R² = 0, 1833), Average November: y = -
0.0483x + 107.88 (R² = 0.1376).

Fig. 3 -    Trends in bud burst and flowering dates at the Sidi Lakhdar (SD) 
and Benchicao (MD) sites. *, ** indicate the significance level of 
the correlation for P<0.05 and for P<0.01, respectively. Sidi 
Lakhdar: (SD) Bud burst/years: y = 0,1397x + 80, 86 (R² = 0, 
0104), Flowering/years: y = -0.4412x + 105.03 (R² = 0.0872). 
Médéa: (MD) Bud burst/years: y = 0.7623x + 83.257 (R² = 
0.2496), Flowering/years: y = 0.8971x + 100.4 (**R² = 0.3263).



Adv. Hort. Sci., 2019 33(3): 417-431

424

liest years being 2003, 2009, 2010 and 2011, and the 
later years 2001, 2004 and 2005 At Benchicao site, a 
significant tendency (P = 0.010) at the late flowering 
dates of the apple tree is to be reported (Fig. 3b). On 
the other hand, differences in historical trends were 
shown in the bud break dates, oscillating between 
advancement during the years from 2000 to 2003, 
and a delay in the years 2004 to 2008. 

Accumulation of chilling units in winter 
     The Utah cold unit (CU) accumulation curves 
reveal significant interannual differences at the Sidi 
Lakhdar site and show that for the years 2001, 2007, 
2010 and 2016, this accumulation was insufficient 
because at below 600 CU, which is well below the 
estimated needs of the Golden Delicious variety (900 
CU) (Fig. 4). On the other hand, at mountain site of 
Benchicao, the needs are always quickly satisfied. 
     In order to analyze the influence of the different 
months in terms of cold units, we calculated the cor-
relations between the dates of bud burst or flowering 
and the monthly temperatures (minimum, average 
and maximum) (Table 3). Very schematically, the ten-
d e n c i e s  c a n  b e  s u m m e d  u p  a s  f o l l o w s :  A t  t h e 
Benchicao site, the month of January and the whole 
period from November to January and February have 
a strong influence on meeting the needs in cold units 
because the correlation is positive (the warmer it is, 
the more the budding/flowering is late), whereas it is 
not the case in November and December (October 
remains quite neutral with a negative correlation). 
The impact of January is preponderant because if we 

look at the influence of the period from November to 
January, we find a negative effect of high tempera-
tures on the precocity (R² = 0.40) while the months of 
November and December have an inverse effect. 
     At the site of Sidi Lakhdar, the balance sheet is 

Fig. 4 -  Cumulative cold unit according to the Utah model at the 
Sidi Lakhdar site. A) Years when cumulative cold is less 
than 500 hrs; B) Years when cumulative cold exceeds 800 
hrs.

Table 3 - Spearman's correlation between bud burst and flowering for ‘Golden delicious’ apple tree and mean temperature from 
October to April

* P<0.05, **P<0.01.

Variable

Sidi Lakhdar (SD) Benchicao (MD)

Mean Temperature Minimum Temperature Maximum Temperature Mean Temperature Minimum Temperature Maximum Temperature

Bud burst Flowering Bud burst Flowering Bud burst Flowering Bud burst Flowering Bud burst Flowering Bud burst Flowering

October -0.031 0.11 -0.21 0.13 -0.20 0.033 0.015 0.019 -0.106 0.135 0.081 0.14

November  -0.41 * -0.12  -0.55 * -0.21 -0.38 -0.036  -0.54 * -0.225 -0.57* -0.232 -0.47* 0.18

December -0.18  -0.43 * -0.11 -0.232 -0.2  -0.50 *  -0.40 * 0.054 -0.52* -0.11 -0.322 0.18

January 0.31 * -0.002 0.006 -0.24 0.46 * 0.14 0.46 * 0.3 0.232 0.15 0.54* 0.41

February 0.10 0.01 -0.09 0. 12 0.01 0.13 0.063 0.073 0.021 -0.015 0.13 0.15

March  -0.43 *  -0.34 * -0.27 -0.147 -0.36  -0.36 *  -0.60 *  -0.65 * -0.60* -0.64* -0.55* -0.56*

April  -0.45 * -0.30  -0.41 * -0.145  -0.48 *  -0.33 * 0.08 -0.072 -0.101 -0.30 0.12 0.041

November-January 0.30 * -0.26 0.14  -0.45 * 0.30* -0.30* 0.43 * 0.40 * 0.28 0.33 0.52* 0.53*

November-February 0.06 -0.052 0.21 -0.14 0.18 -0.14 0.48 * 0.44* 0.233 0.212 0.30 0.21

November-March 0.041 -0.29 0.01 -0.20 0.132 -0.30 0.184 0.27 0.062 0.104 0.33 0.30

March-April  -0.56 *  -0.45 * 0.08 -0.025  -0.54 * -0.330 -0.26 -0.44* -0.304 -0.54* -0.133 -0.20



Abed et al. ‐ Climate change effect in apple flowering

425

globally the same. The correlations between mean 
and maximum temperatures in January on the one 
hand, and bud break dates on the other, are signifi-
cantly positive, indicating the importance of this 
month’s temperatures for the satisfaction of cold 
unit requirements, the month of October remains lit-
tle determinant. A hot January is a delay in meeting 
cold needs and bud break. A negative tendency of 
the high temperatures of the period from November 
to January on the precocity (R2 = 0.30) was recorded 
whereas the other months go rather in the direction 
of a gain of precocity. Significant and negative rela-
tionships were observed between maximum temper-
atures in December and flowering, with a correlation 
coefficient of -0.50. 

Accumulation of forcing units in spring 
     March-April period (-0.44) show the link between 
the early flowering period and the average tempera-
ture It is rather March that plays the main role for 
both sites. At the Benchicao site, only March temper-
atures show a significant negative correlation with 
bud break and flowering dates. Negative correlations 
obtained between average temperatures of the peri-
od, with a very high prevalence of March tempera-
tures. At the site of Sidi Lakhdar, March and April 
strongly influence the precocity via maximum tem-
peratures and average temperatures. 

Phenology modeling 
     For both sites, the best sequential models selected 
are given in Table 4. They were chosen on the basis of 
efficiency (EFF) and RMSE (RMSE), but also taking into 
account the physiological relevance of the tempera-
ture response curves for the cold unit stacking phase 
and the heat unit stacking phase. RMSE may appear 

acceptable (~ 5 days) on a flowering date but the effi-
ciencies are less good. The correlation between the 
observed values and the predicted values confirms 
this diagnosis (Fig. 5). The efficiency is very slightly 
improved (reaching a difference of 0.03 to 0.09) by 
eliminating the years when the cumulative cold units 
are not satisfactory at Sidi Lakhdar site. 

Table 4 - Modeling bud burst and flowering for ‘Golden delicious’ apple tree by Chuine/Wang and Smooth Utah/Sigmoid in the two stu-
died sites with all years and without years where chilling does not satisfied

Site Two sites with all years
Two sites without years where chilling dose not  

satisfied, 2001, 2007, 2010, 2016

Phenological stage Bud burst Flowering Bud burst Flowering
Model Chuine / Wang Smooth Utah / Sigmoid Chuine / Wang Smooth Utah / Sigmoid
T0 starting date -107.8 -75.3 - 110.6 61.4
RMSE 5.39 4.86 5.93 4.16
EFF 0.49 0.47 0.50 0.56
Settings Chuine Wang Smooth Sigmoid Chuine Wang Smooth Sigmoid

A   0.50 Topt   20.69 Tm1     -37.54 D   -40  A   0.68 Topt   17.09 Tm1   9.72 D   -2.72
Topt   18.45

B   12.70 Tmin   3.30 Topt      23.52 E   6.40 B   -28.90 Tmin    2.40 Tn
2   

27.52 E   -21.80
Min   -0.86

C   27.04 Tmax   43.14 Tn
2      

    24.40 C   -15.36 Tmax  26.36
Min       -0.99

Fig. 5 -  Comparison between the observed and the predicted 
flowering date of apple in two sites. A) for all years by 
the Smooth Utah/Sigmoid model. y = 0.5286x + 49.199; 
R² = 0.4796; B) without the years where the cumulative 
cold units are not satisfied by the Smooth Utah/Sigmoid 
model. y = 0.5041x + 51.647; R² = 0.5555.



Adv. Hort. Sci., 2019 33(3): 417-431

426

     By examining separately the two sites, and in par-
ticular that of Sidi Lakhdar, which shows years when 
the accumulation of cold units is not satisfied (Fig. 
6a), we see that the withdrawal of these years great-
ly improves the results of modeling (Fig. 6b) and in 
p a r ti c u l a r  f o r  fl o w e r i n g .  T h e  r e l e v a n c e  o f  t h e 
response curve obtained for the cold unit function is 
also greatly improved (Table 5). 

     At Benchicao site (Table 6), the efficiency of the 
two-phase model is medium and figure 7 shows that 
it is difficult to predict the early years. In fact, the 
two-phase model is not much better than a one-
phase model on bud break and not better for flower-
ing. The results of the one-phase model (only the 
heat-accumulation model: degree-day growth, 
Parabolic, Richarsdon, Wang, Sigmoid, Threshold and 
Smooth Utah) yielded non-significant results. 
 
 
4. Discussion and Conclusions 
 
     The sensitivity of phenophases to temperature 
changes is a good indicator of the long-term biologi-
cal impacts of climate change and terrestrial ecosys-
tems (Richardson et al., 2013). Several studies have 
shown that the phenophases most sensitive to tem-
perature variations are those occurring in spring or 
summer and that there is a relatively linear relation-
ship between the occurrence of these phenophases 

Site Sidi Lakhdar with all years
Sidi Lakhdar without years where chilling dose not  

satisfied, 2001, 2007, 2010, 2016

Phenological stage Bud burst Flowering Bud burst Flowering

Model Chuine/ Sigmoid Chuine/ Sigmoid Chuine/ Sigmoid Chuine/ Sigmoid
T0 -102.3 61 -119 -59.7

RMSE 3.79 5.02 3.30 2.10
EFF 0.72 0.44 0.80 0.90

Settings Chuine Sigmoid Chuine Sigmoid Chuine Sigmoid Chuine Sigmoid
A   1.61 D   -32.51 A   2.95 D   -11.93 A   0.96 D   -2087 A   3.21 D   -40

B   - 5.67   E   -21.66 B   -25.47 E   0.50 B   -29.7 E   -25.47 B   12.47     E   14.93

C   19.42 C   8.60 C   -6.72 C   16.93

Table 5 - Modeling bud burst and flowering for ‘Golden delicious’ apple tree in Sidi Lakhdar by Chuine/Sigmoid model with all years and 
without years where chilling does not satisfied

Table 6 - Modeling bud burst and flowering for ‘Golden deli-
cious’ apple tree in Benchicao by Smooth Utah/Wang 
and Chuine / Sigmoid models with all years

Fig. 6 -  Comparison between the observed and the predicted 
bud burst date of the apple tree at the Sidi Lakhdar site. 
A) for all years by the Chuine/Sigmoid model. y = 0.8316x 
+ 13.544; R² = 0.7207; B) without the years when the 
c u m u l a t i v e  c o l d  u n i t s  a r e  n o t  s a t i s f i e d  b y  t h e 
Chuine/Sigmoid model. y= 0.8165x + 15.548; R² = 0.8066.

Site
Benchicao with all the years

Phenological stage Bud Burst Flowering

Model Smooth Utah / Wang Chuine / Sigmoid

T0 -104.9 -78.7

RMSE 5.43 4.91

EFF 0.48 0.46

Settings Smooth Utah Wang Chuine Sigmoid

Tm1 -34.85 Topt    22.31 A        0.45 D    -39.99

Topt    21.15 Tmin   3.60 B      -10.58 E      6.39

Tn2    29.42 Tmax   49.9 C        1.03

Min    -0.81



Abed et al. ‐ Climate change effect in apple flowering

427

and temperature (Gordo and Sanz, 2010; Morin et 
al., 2010; Beaubien and Hamann, 2011). 
     Our study is a first attempt to evaluate the impact 
of global warming on the bud break and flowering of 
the apple tree in northern Algeria. The study of the 
chronological series of temperatures (minimum, 
average and maximum) from 1980 to 2016 (36 years) 
in the two important apple production sites, namely: 
Sidi Lakhdar and Benchicao, showed a very significant 
warming in October and April at the site of Sidi 
Lakhdar (SD) likely to strongly disrupt the entry into 
endodormancy and ecodormancy. Strangely, the 
Benchicao (MD) site does not show global warming 
and even a cooling trend in November and February, 
which could lead to an endodormancy and a start of 
satisfaction in cold units and then an acceleration of 
the recovery of growth leading to greater precocity. 
     Establishing the time of endodormancy emer-
gence is important (Guerriero et al., 2002), but is 
hampered by the complexity of the process, including 
the fact that, under natural conditions, cold and 
warm temperatures alternate, causing “Inversions” in 
the process of endodormancy emergence (Overcash 
and Campbell, 1955; Couvillon and Erez, 1985; Erez 
and Couvillon, 1987). Some results suggest that par-
tial dissatisfaction with cold can be compensated by 
heat unit supplementation for bud break (Dantec, 
2014). 
     To lift the endodormancy, the bud must accumu-
late enough cold (Campoy et al., 2011). When the 
plant has reached its cold needs, the endodormancy 
is lifted and the buds can resume their growth as 
soon as the conditions become favorable, i.e. under 
certain (rather high) temperature conditions, soil 
moisture and nutrients, and for photosensitive 

species, certain photoperiod conditions (Körner and 
Basler, 2010; Polgar and Primack, 2011). These favor-
able conditions must last for a certain period of time 
for the bursting of the buds to appear. 
     For our case, the cold needs were always met to 
lift the endodormancy of the apple tree at the 
Benchicao site, and this as from the end of December 
or the first half of January (Fig. 4). Conversely, at the 
Sidi Lakhdar site, values below the threshold for sat-
isfying cold needs estimated at 900CU for the Golden 
Delicious apple tree were obtained for the years 
2001, 2007, 2010 and 2016. When it takes place, the 
satisfaction of cold needs is later, around mid-
February (Fig. 4) and does not really start until the 
end of November. Everything leads to a dominating 
importance of the month of January in the course of 
the endodormancy lifting process and it will be inter-
esting to look at what the future climate scenarios 
give for this particular period for the choice of future 
apple varieties. 
     The months of November and December play a 
precocious role at the Benchicao site (negative corre-
lation with the date of bud burst or flowering). This 
can only be understood if the organogenesis in the 
buds continues during these two months and there-
fore there is no endodormancy at this time. The 
observed increase in average November and October 
minimum temperatures (Table 2) is consistent with 
this. At the site of Benchicao, the month of March is 
crucial for the precocity, it is the temperatures of this 
month which allow the growth after the satisfaction 
of the needs of cold towards the end of December 
and the beginning of January all the more so as the 
temperatures of the February remain rather low (and 
tend towards a cooling). The tendency to tardiness 
with the site of Benchicao is thus coherent with the 
cooling in the month of February. The October warm-
ing at Sidi Lakhdar site may explain later entry into 
endodormancy. Gentle temperatures (12°C) in 
February can then accelerate bud burst and flower-
ing, at least for years when cold needs are met. 
Otherwise endodormancy will be greatly delayed or 
disrupted. According to the study of Legave et al. 
(2015), carried out in three geographically contrast-
i n g  c o u n t r i e s  o f  t h e  M e d i t e r r a n e a n  r e g i o n ,  i n 
Morocco (Meknes), France (Nimes) and Italy (Forlì) 
over the last 40 years in order to understand the 
impact of climate change, especially the increase in 
temperature, on the Golden Delicious apple tree, the 
forcing period is shorter in Meknes. Legave et al. 
(2012) also found a marked trend towards shorter 
s i m u l a t e d  d u r a ti o n  o f  f o r c i n g  p e r i o d  a n d  l a t e 

Fig. 7 -  Comparison between the observed and the predicted 
flowering date of the apple tree at the Benchicao site by 
the Chuine/Sigmoid model. y = 0.4501x + 57.365; R² = 
0.4632.



Adv. Hort. Sci., 2019 33(3): 417-431

428

endodormancy period. The physiological functioning 
of the Golden Delicious apple tree during the dor-
mant and growing season may explain, in part, the 
regional differences observed in the flowering dates 
(Heide, 1993). In the same context, Kauffman and 
Blanke (2018) have reported after a study conducted 
on three cherry cultivars at different levels of cold 
needs (minimum, medium and high) that, in optimum 
chill, the optimum forcing was ca. 8.000 GDH (>12 
°C), irrespective of variety, allowing up scaling of the 
results to possibly other varieties. Overall, the results 
have shown that diminishing chilling as a result of cli-
mate change can be compensated for, in part up to 
50%, by a larger amount of forcing to obtain natural 
flowering in the orchard. These results may explain 
the good progress of flowering on the site of Sidi 
Lakhdar, although the cold needs were not often sat-
isfied. El Yaacoubi et al. (2014) also reported that 
spring temperatures appear to be essential for com-
plete flowering in mild climates. In the latter case, 
early full flowering dates occurred when the average 
t e m p e r a t u r e  d u r i n g  t h e  f o r c i n g  p e r i o d  r a p i d l y 
exceeded 15°C provided adequate satisfaction of the 
cold requirements. Phenological models predicting 
the occurrence of different phenophases as a func-
tion of environmental conditions (mainly tempera-
ture and photoperiod), predict that the global 
increase in temperature during the winter will slow 
or even jeopardize the endodormancy emergence 
due to lack of cold (Chuine et al., 2016). The one-
phase and two-phase models for all years do not give 
good results at the Sidi Lakhdar site. This is explained 
by the negative influence of years when cold unit 
n e e d s  h a v e  n o t  b e e n  m e t .  I f  t h e s e  y e a r s  a r e 
removed, the two-phase Chuine/Sigmoid model for 
bud burst and flowering gives good results. This may 
mean that in these cases of partial non-fulfillment of 
cold unit requirements, the physiological processes 
involved in bud break-up and flowering are different 
or that “something” in addition occurs. At Benchicao 
site, the efficiency of the two-phase models is aver-
age, since the requirements in cold units are often 
met; only the forcing period can have an effect on 
the precocity. 
     This study aimed to show the effects of the antici-
pated increase in temperature on two phenological 
phases of the apple tree (Golden Delicious) in two 
Algerian sites with contrasting climates. We high-
lighted contrasting trends by site and by period. 
Warming at Sidi Lakhdar site in autumn and spring, 
however, the statistical data of temperatures did not 
raise any average warming at the Benchicao site. 

Rather surprising and never described before, there 
has been a tendency to cool down some months at 
the Benchicao site. Critical periods for cold units 
were identified, concerning the period between 
November and January at Benchicao site, but January 
t e m p e r a t u r e s  w e r e  m o r e  i m p o r t a n t  i n  l i ft i n g 
endodormancy. At the site of Sidi Lakhdar, buds 
enter late into endodormancy and the result is a late 
action of cold that extends until February without 
always being sufficient. Forced side, it is the tempera-
tures of the month of March that have a discriminat-
ing effect on bud burst and flowering at the site of 
Benchicao combined with those of April at the site of 
Sidi Lakhdar. On this site, despite the warming in 
April, we do not gain in precocity probably because 
of a satisfaction of cold needs “to the limits” as 
describe Legave et al. (2012) for the Nimes region. 
We have also highlighted, particularly at the site of 
S i d i  L a k h d a r  t h a t  m o r e  c o m p l e x  p h y s i o l o g i c a l 
processes must be at work especially the years of low 
cumulative cold units. It is not excluded that other 
factors, not included in this work, could be involved 
in the budburst process such as photoperiod or pre-
cipitation (Vitasse et al., 2009; Grab and Craparo, 
2011; El Yaacoubi et al., 2014). Except for the two-
phase Chui ne/Si gmoi d budburst and floweri ng 
model, which gave better results at Sidi Lakhdar site 
after the elimination of the years when the cold unit 
requirements were not met, all the models give 
rather weak efficiencies indirectly confirming the 
non-taking into account of a complexity of factors 
associated with physiological functioning for sites like 
Sidi Lakhdar’s. 
     The study of the impact of global warming on the 
apple tree requires a precise determination of the 
accumulations in cold units necessary for the emer-
gence of endodormancy and budding in various envi-
ronments. This involves highlighting these two phas-
es by forcing techniques at the laboratory level and 
anatomical studies of meristematic bud tissues to see 
their ability to bud. 
 
 
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