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JCBPS; Section B; August 2016 – October 2016, Vol. 6, No. 4; 1258-1281, E- ISSN: 2249 –1929

Journal of Chemical, Biological and Physical Sciences

An International Peer Review E-3 Journal of Sciences

Available online atwww.jcbsc.org

Section B: Biological Sciences

CODEN (USA): JCBPAT Research Article

1258 J. Chem. Bio. Phy. Sci. Sec. B, August 2016 – October 2016; Vol.6, No.4;1258-1281

Phenological monitoring of cork oak in Kroumirie

(northwest Tunisia)

Kaouther Ben Yahia* 1.4

, Hatem Chaar 2, Salima Bahri

1, Sameh Mhamdi

1.4,

Kamel Soudani 3, Ali Khouaja

4, Brahim Hasnaoui

4

1Laboratoire d’Ecologie forestière, INRGREF, BP10, Ariana, 2080, Tunisia

2 Laboratoire des Ressources Sylvo-pastorales de Tabarka, ISP Tabarka

3 Laboratoire Ecologie Systématique et Evolution, UMR8079, Université Paris-

SudXI, 91405 Orsay, France.

4 Laboratoire des Ressources Sylvo-pastorales de Tabarka, ISP Tabarka.

Received: 21 September 2016; Revised: 08 October 2016; Accepted: 14 October 2016

Abstract: The phenology of Quercus suber L., a dominant sclerophylious

species in northwest Tunisia, was studied for two years at three sites selected

according to altitudinal gradient. The seasonal progression of phenological

events was analyzed on 41 trees in Ain Snoussi, 39 in Bellif and 22 in

Khroufa selected from 1ha plots. Phenological observations about budburst

and flowering were made every week from mid-March to late May, about leaf

fall from January 2010 to the end of December 2011. Litter fall was estimated

at plot level. 35 litter traps were placed every 15 m. Statistical models (linear

logistic model) were used to analyze the following: i) the kinetics of early

bud break and full bud dates (d1 and d2); ii) the beginning and end of

flowering (F0 and FF) and iii) the two leaf fall peaks. Bud break, flowering

and leaf fall showed strong seasonality. The first two phenological phases

(bud and bloom) occurred in the spring while the third took place in both

spring and autumn but with different growth rates. The median dates of early

bud break and full bud estimated from the model showed that cumulative

needs bud burst at higher elevations occurred later than at lower altitudes

assuming that cumulative needs in degree days have been met. Leaf fall is

usually in two phases, presumably explained by the rhythmic nature of the

Phenological … Kaouther Ben Yahia et al.

1259 J. Chem. Bio. Phy. Sci. Sec. B, August 2016 – October 2016; Vol.6, No.4; 1258-1281.

primary growth of this species, making its kinetics well-fitted to a bi-Richards

model (sum of two Richards-Chapman models). Phase 1 of leaf fall, which

was the most important, is synchronized with budding and flowering. All

these periods have coincided with wet months, during which the trees have

renewed almost 90% of their foliage.

Keywords: Cork oak, phenology, bud burst, flowering, leaf fall, statistical

models

INTRODUCTION

Phenology is the study of periodic phenomena (flowering, leafing, fruit, autumnal yellowing

and leaf fall) in plants. It especially tries to grasp the progress of temporal, spatial and

stational recurrence of these phenomena1,2

and also study the factors that influence 2,3. These

phenomena are genetically predetermined but also strongly modulated by environmental

conditions 4. The main environmental factors affecting these phenomena in plants are

temperature 2, 5,6

, photoperiod and water availability6. Many previous studies

2,7-9 have shown

the effect of temperature on early bud development of temperate forest species and how this

is especially related to early winter and mild spring temperatures and interannual variations.

Studies in boreal and temperate environments 2,10-13

showed that regardless of the species, bud

burst at higher elevations occurred later than at lower altitudes. In addition, these studies

showed that the date of bud break is also correlated to photoperiod. In Mediterranean species,

the date of bud break is determined by temperature, photoperiod and water availability5, 14, 15,

.

In recent decades, climate change observed in many parts of the globe2, 11, 16

could have had a

considerable impact on the phenology and duration of the growing season of plants, and

consequently, on productivity and carbon balance of forest ecosystems 2,17

,18

. The trees,

which cannot react quickly to these changes (especially due to the increase of the

temperature), would become less adapted to their local climate. Thus, in many studies on the

evolution of phenological stages (budding, budbreak, flowering, and leaf fall deciduous

species and conifers, especially in temperate regions13,

19,

20

, were studied to examine the

possible consequences of climate change. Unfortunately, few studies have investigated the

phenology of sclerophyllous species characteristic of the Mediterranean region in natural

conditions, or variations within the population 21

.

The few studies done were also limited to the northern Mediterranean and mainly concerned

cork oak (Quercus suber L.) and holm oak (Q. ilex L.) 5,21-26

, and the phenology of cork oak

seedlings (Q. suber L.), Zeen (Q. canariensis Willd.) and afares (Q. afares Pomel) grown in a

nursery in Tunis, not in situ Mhamdi 27

. El Nennejeh28

was also interested in the study of

phenology and growth of various populations of cork oak under stress conditions in the

nursery, far from their original site. It would be interesting to conduct studies on oak stands,

especially cork oak, a native species, which holds both an ecological as well as economic and

social interest, in its natural habitat in Tunisia (Kroumirie and Mogods).

Given our ignorance of the phenology of cork oak, a Tunisian evergreen species, and the

growing interest of these observations in the context of potential effects of global warming,

the objective of this work is to characterize the phenological events (vegetative buds,

flowering and leaf fall) and their spatiotemporal and individual variability.



MATERIAL AND METHODS

Study zone: The study area is located in nnorthwest Tunisia. Three 1-hectare northern

exposure plots of cork oak from the uneven-aged forests of Bellif, Khroufa and Ain Snoussi

were selected according to an altitudinal gradient to carry out phenological monitoring. All

plots were in a low humidity bioclimatic zone, mild in Bellif and Khroufa and temperate in

Ain Snoussi. A detailed description of the plots is located in Table 1.

Table 1: Characteristics of the three study sites

Site characteristics Ain Snoussi Bellif Khroufa

Latitude 36° 48’23N 37° 02’ 22.8’’N 36°56’33.8’’N

Longitude 008°53’58.6E 009° 04’ 43.6’’E 008°57’39.4E

Altitude (m) 612-633 70 et 110 182-214

Slope (%) 19 13-42 24%

Vegetation

Stem number (stems/ha) 412 237 168

Height (m) 7.18±2,072 12.6±2,163 9.69±2.4107

DBH (cm) 24.5±9,85 40.56±12,84 37.204±14.04

Age (years) - 66 86

basal area (m²/ha) 27.86 27.15 20.83

arboreal stratum Q. suber + Arbutus unedo + Q.

faginea (dominated species)

Q. suber (97.5%) + Q.

faginea (2.5%)

Q. suber (91,7%)+Q. faginea

(8,3%)

Shrub stratums Arbutus unedo, Myrtus

communis

Erica arborea, Myrtus

communis, Phillyrea

angustifolia, Pistacia

lentiscus

Erica arborea, Myrtus

communis, Pistacia lentiscus,

Smilax aspera,Quercus

coccifera

herbaceous stratum annual species Pteridium aquilinum+

annual species

annual species (Briza

maxima)

Soil

Type of soil red soil leached ground red bruned soil brown soil

clay (%) 51.2±18.52 30.75± 10.53 15.75±6.84

Silt (%) 28.25±8.61 32±4.96 14.5±1.732

Sand (%) 17.75±9.74 35.5±6.35 64±7.118

soil texture clayey silty sandy sandy-silt sandy clayey silt

Bed rock clay clay sandstone

%MO 2.25±2.59 1.65±0.51 0.77±0.38

AWC

Maximum available water

content (mm)

128 145.8 126

Da (g/cm3) 1.355±0,109 1.506±0.133 1.679±0.08

The average annual temperature in 2010 and 2011 was 18.04°C, 17.14°C and 12.8°Cin Bellif,

Khroufa and Ain Snoussi, respectively. Over those two years, the average annual rainfall was

1083.9, 1028.2 and 1324.95 mm in Bellif, Khroufa and Ain Snoussi, respectively.

Automatic recording meteorological stations were set up in a forestry center triage located 0.5

km from the study sites. Temperature and precipitation measurements were taken in half hour

increments.

Phenological study: Phenological monitoring was done over a period of two years, 2010

and 2011. The phenological stages (early bud break and full bud, early and late flowering and



leaf fall) were recorded on 41, 39 and 22 trees in Ain Snoussi, Bellif and Khroufa,

respectively.

Vegetative buds and flower buds were monitored weekly from March 12 until the end of May

during the two seasons in 2010 and 2011. For study stations, observations were made on the

same day by the same observer using binoculars. Buds were observed according to the scale

set by Salmon24

who defined six stages of bud development (Figure 1). Buds were said to

have been observed when they were opened and at least one young leaf or needles had

appeared (D stage). Two dates were identified for the tree as well: 1) the date of early bud

break (when 10% of the crown buds had reached stage D); and 2) the full bud date (when

90% of the crown buds had reached stage D). Bud duration was thus calculated as the

difference between the two dates. For each plot, the two median dates for start of and full bud

break were calculated.

Figure 1: Stages of leaf bud break of Quercus suber L. Stage A bud completely closed; Stage

B, Bud lengthened with no unstuck scales; Stage c, Bud soft starting to detach scales; Stage

C, Bud opened with open scales; Stage D, bud blossomed with already unfolded leaf; Stage

E, Bud crooked, several leaves folded (leaf expansion).

The flowering date was visually identified by the appearance of male and female flowers in

the spring of 2011.

Each study plot was equipped with 35 litter traps (1m²) 29

located every 15 m. These traps

were raised slightly off the ground to avoid contamination 30,

31

. They are used to recover all

the lost parts of trees and shrubs fallen to the ground: leaves, fruits, flowers, bark and twigs.

Pickup was weekly and done the same day as the phenological observation. The litter

collected from each trap was separated into its various components, then left to dry in an oven

at 75°C for 48 hours to constant weight (Figure 2).

Stade DStade C Stade E

Stade B Stade cStade A



Figure 2: Ombrothermic diagram of Bagnouls and Gaussen (P = 2T) for the two years 2010

and 2011 and the three sites (A) Bellif, (B) Khroufa and (C) Ain Snoussi.

Statistical Analyses: A logistic model was used 32

to analyze the four phenological stages:

(1) early bud break or budburst onset, BBO; (2) full bud or full-budburst, FBB; (3) early

flowering or blossoming onset, BLO; and (4) full-blooming or blossoming, FBI. This model

was used to analyze the proportion of trees p having reached the phenological stage studied.

The link function between the expectation of this proportion π p (between 0 and 1), the linear

predictor formulated from the explanatory variables (site and season, as variables, and time t



as a quantitative variable, as well as interactions between these variables), is the function

logit (π) = log (π / (1-π)). The linear logistic model used is written as:

p =exp(+' x)

1+exp(' x)..2

log it () = log ='x

1-..1

Where:

Where is the ordinate at the origin (intercept) and = (1....s) is the vector of slope s .

With the logistic model used, the error is assumed to follow the Bernoulli distribution, as the

treated variable is binary (1: Tree having reached the stage in question; 0: otherwise).

The model inflection point is reached at time = T_i -α/β which corresponds to p_i = 0.5. This

is in fact the median (time when 50% of the trees have reached the stage in question).

The asymptote of the model (1) is equal to 1. However, for two stages BLO and FBI

(beginning and full bloom), only a certain percentage of trees have reached these stages

(asymptote is therefore different from 1). To remedy this problem, the model (1) was adjusted

using only the trees having flowered. Asymptotes (different from 1) were estimated from the

ratio number of flowering trees on the total sample trees, and were compared using the linear

logistic model and the site and season as explanatory qualitative variables.

The quality of the adjusted logistic model was assessed using McFadden's pseudo-R2

parameter proposed in 1974:

(3)

Where = Model with predictors

= Model without predictors

= Estimated likelihood.

As for leaf fall, a preliminary review showed that the accumulation of leaf fall over time t

(from January 1st of the current season), expressed in g / m², is usually held in two phases of

sigmoidal shape, sometimes interspersed by a temporary slowdown. This accumulation of

leaf fall over time t cannot be adjusted by a single sigmoidal model, but rather by the sum of

two models; each model adjusting the accumulated leaf fall over time for a single phase. The

preselected individual model (for one phase i) is the Richards-Chapman model because it is

more flexible33

. It can be written as 34

:

(4)

Where A: asymptote, m: shape parameter (sigmoidal curve when it is positive) K: maximum

relative growth rate per unit of time (i.e., slope at an inflection) and T_i: time at the inflection



point. The inflection point is the point (T_i, Am ^ (1/ ((1-m)))) 34

. The logistic model is a

special case of the Richards-Chapman model where m = 2.

From this model other quantities derived can be estimated: the beginning and end of the leaf

falling phase (time required for there to be a 10% or 90% accumulation of leaf fall of the

asymptotic A), the duration of the leaf fall period (the time interval necessary for there to be

an accumulation of leaf fall between 10 and 90% of the asymptotic A), and the maximum

increase in leaf fall (dy / dt T_i time).

Thus the Bi-Richards model for modeling the accumulation of leaf fall is:

(5)

The correlation measures over time in the traps were taken into account by specifying the

structure of the covariance matrix of the residues R (type AR (n)) 35

.

The quality of the adjustment of the model (5) was evaluated using: 1) the Pseudo coefficient

of determination (R2), 2) the Pseudo adjusted coefficient of determination (adjusted R2) and

3) error (Root Mean Square Error, RMSE), where:

(6)

(7)

(8)

Where yobs and ypréd are the measured and predicted values of the accumulated leaf fall,

respectively; n: the number of observations; and p: the number of model parameters.

Analyses were performed using the procedures Proc logistic, proc model and Proc nlmixed

SAS version 9.3 36

.

RESULTS

Meteorological data: Average annual temperatures in Ain Snoussi and Bellif were slightly

higher in 2010 (12.96°C and 18.13°C, respectively) than in 2011 (12.57°C and 17.87°C,

respectively) whereas Khroufa remained constant in both seasons (17.11°C and 17.09°C).

However, rainfall was greater in 2011 than 2010 in all three study sites. The rainfall reported

was 1307.81mm, 1003.8 mm and 1014.3 mm in Ain snoussi, Bellif and Khroufa,

respectively, in 2010, while in 2011, it was 1342.1 mm, 1164 mm, and 1042.1 mm in Ain

snoussi, Bellif and Khroufa, respectively.

Over the two years of observation, the rainfall was type AHPE for the Ain Snoussi and Bellif

stations, whereas it was type HAPE in the Khroufa station (Figure 3). Following the

Bagnouls and Gaussen’s Ombrothermic diagram in 2010, drought occurred between June and

August in Ain Snoussi and Khroufa, respectively, and between April and August in Bellif. In



2011, it lasted from May to August in Bellif and Khroufa and from June to August in Ain

Snoussi.

Figure 3: Kinetics of observed dates of the beginning of bud burst (stage d1) (A, Bellif; B,

Khroufa C, Ain Snoussi) and end bud (stage d2) (D Bellif; E, Khroufa; F, Ain Snoussi) of

Quercus suber L. in the three study sites, and adjusted logistic models

Early and full bud (d1 and d2): The analysis of phenological variability was primarily

based on visual observation. A median date was estimated for each site and year, using the

logistic model. This median date represented the date when 50% of the sampled trees were in

the studied stage.



For both campaigns of observations and for the three stations studied, the early and full bud

for the majority of trees lasted from March to the end of April. Statistical analysis using the

logistic model showed that for the start date of bud burst (d1), there was a site effect, time

effect and a significant interaction year * Site (Table 2). However, there was no significant

effect due to year. As to the date of bud burst (d2), analysis showed significant effects for day

and year and interaction year*site. However, there was no significant site effect or significant

interaction between day * site. The logistic model was adjusted for both dates (d1 and d2)

removing non-significant effects. The goodness of fit was great (McFadden's pseudo-R2 of

0.7257 and 0.5727 for both steps d1 and d2, respectively).

Table 2: Deviance analysis using the logistic model, applied to variables beginning of bud

burst (d1), end of bud break (d2), onset flowering (F0) and end of flowering (FF): pr (chi-

square).

Effets testés d1 d2 F0 FF

Site <0,0001 0,0064 0,0799 0,0925

Time <0,0001 <0,0001 <0,0001 <0,0001

Time x Site <0,0001 0,0038 0,1135 0,0293

Year 0,1871 0,3977 - -

Year x Site <0,0001 < 0,0001 - -

In 2010, the median date of start of bud burst (step d1) estimated from the model was found

to be March 20 (79.04 ± 0.75 j: number of days from January 1, 2010 ± SE) for Bellif and

March 24 (83.30 ± 0.89 j) for Khroufa. This date was a little later at the Ain Snoussi station

(April 8; 97.67 ± 0.70 j) (Table 3). However, there was no significant difference in median

dates for stage d1 between Bellif and Khroufa, although there was a lag of 4.26 ± 1.16 days.

The difference between median dates was very highly significant (p <0.0001) between Ain

Snoussi and Bellif and between Ain Snoussi and Khroufa, and the differences were more

significant (18.62 ± 1.02 d and 14.36 ± 1.13 days, respectively). The value of k rate

(controlling the slope in the middle) at stage d1 was independent of the site, and also of the

year, with a value of 0.3302 ± 0.0197 tree / day (Figures 3A, 3B and 3C). Thus, most of the

trees at the three sites had approximately the same time to reach stage d1.

For the year 2010, the median date of full bud (stage d2) occurred on March 26 (85.93 ± 0.65

j) in Bellif, on April 1 (90.57 ± 0.74 j) in Khroufa and April 17 (107.24 ± 0.91 j) in Ain

Snoussi. Although these dates seem very close together, there were very highly significant

differences between them (p <0.0001). The value of k rate (controlling the slope in the

middle) at stage d2 was however dependent on the site, but not on the year; Khroufa’s site

had the highest k value (0.3723 ± 0.0499 tree / d) but was not significantly different from

Bellif (0.3302 ± 0.0287 tree / d). However, that of Ain Snoussi was the lowest (0.2262 ±

0.0191 tree / d) and significantly different from the other two. Thus, the majority of trees in

Khroufa and Bellif took less time to reach stage d2, compared to those in Ain Snoussi

(Figures 3D, 3E and 3F).



Figure 4: Non-flowering trees at the study site: proportion ± confidence interval.

The bud duration (difference between median dates of the two stages d2 and d1) in Bellif and

Khroufa was about 7 days, while in Ain Snoussi, it was about 9 days.

This stational inter-variability of start and full bud dates appears to be due to the altitudinal

gradient. In addition, linear regressions between altitude and the dates of beginning of bud

burst (d1) (t = 75.93 + 0.034Altitude; R² = 0.9983) and full bud (d2) (t = 82.24 +

0.0398Altitude; R² = 0.9991) were determined. Strong significant correlations at the 5% level

between the start date of bud burst (d1) and the date of full bud (d2) (correlation coefficient

Pearson R = 0.99946, p = 0.0210); between early bud burst (d1) and altitude (R = -0.9991,

p = 0.0484); and finally between the date of full bud (d2) and altitude (R = 0.99907, p =

0.0275) were also found.

In 2011, the beginning of bud burst (d1) was observed on April 3 (93.38 ± 0.71 j) in Bellif, on

April 1 (91.82 ± 0.96 j) in Khroufa and on April 8 (98.97 ± 0.69 j) in Ain Snoussi. The lag

between Bellif and Khroufa was not significant (1.56 ± 1.19 days) but was highly significant

between Ain Snoussi and Khroufa (7.1556 ± 1.18) and between Ain Snoussi and Bellif

(5.5922 ± 0.99). Full bud stage (d2) was completed on April 8 (98.57 ± 0.88 j) in Khroufa,

April 16 in Ain Snoussi (106.18 ± 0.87 j) and finally April 18 (108.27 ± 0.75 j) in Bellif.

Statistical analysis showed that the trees of the two populations of Bellif and Ain Snoussi

reached the full bud stage d2 together with a non-significant difference of 2.09 ± 1.15 days.

This confirms the lack of correlation between altitude and start dates and full bud in 2011 for

the three stations studied. The population of Khroufa reached this stage earlier than the other

two with a lag of 9.69 ± 1.16 days after Bellif, and 7.60 ± 1.24 days after Ain Snoussi.

Moreover, the differences were highly significant (p <0.0001) between Khroufa and the two

other stations.

It should be noted that the early bud stage d1 shifted 14.33 ± 1.03 days in Bellif, 8.512 ± 1.3

d in Khroufa and 1.30 ± 0.99 days in Ain Snoussi between 2010 and 2011. Indeed, this

variability is very highly significant (p <0.0001) for both Bellif and Khroufa stations, but not

significant for Ain Snoussi.

P, Bellif, 0.23077

P, Khroufa, 0.09091

P, Snoussi, 0.26829 P, Tous sites

confondus, 0.21569

no

n-f

low

rin

g-tr

ees

(%)

Site



As for the full bud stage d2, it also shifted 22.33 ± 0.99 days in Bellif, 8.01 ± 1.15 d in

Khroufa but only 1.07 ± 1.26 d in Ain Snoussi. Similarly, this variability was also very highly

significant (p <0.0001) for both Bellif and Khroufa stations, but not significant for Ain

Snoussi.

Bud duration lasted 7 days in Ain Snoussi and Khroufa, and 15 days in Bellif.

Taking 8°C as the base temperature 37

, the individual populations of Bellif and Ain Snoussi

accumulated 348.5 and 153.6 degree days during the 2010 season (from January 1 to the

median date of the stage in question), from bud start (stage d1) while those of Khroufa,

accumulated 297.6 degree days. To reach the full bud stage (stage d2), the Bellif population

accumulated the most temperatures (405.5 degree days), followed by Khroufa (353.7 degree

days) and finally Ain Snoussi (180.6 degree days).

In 2011, in order to begin to bud (stage d1), the populations of Bellif, Khroufa and Ain

Snoussi had accumulated 349.4, 231.3 and 101.9 degree days, respectively. The full bud

stage (d2) occurred after an accumulation of 453.9 degree days in Bellif, 302.7 degree days in

Khroufa and 125.6 degree days in Ain Snoussi.

Flowering: For the only observation campaign (2011) and for the three study sites, a certain

number of trees did not flower. The percentage of trees with flowers was 73.9% in Bellif,

51.3% in Khroufa and 73.2% in Ain Snoussi (Figure 5). According to the analysis of

deviance, using the logistic model, it was found that the percentage (or proportion) was not

significantly influenced by the site effect (Pr> chisq = 0.2852). However, the difference

between the percentages of flowering trees for both Khroufa and Ain Snoussi sites was

significant at the 0.10 level.

For the three stations studied, the beginning and end of flowering during the 2011 season for

the majority of trees occurred from April - mid-May. The deviance analysis showed that for

the two stages, early (F0) and late flowering (FF), there was a highly significant effect of time

or dates; however the Site effect was significant at the 0.10 level (Table 4). The interaction

Site * time was significant only for the FF stage. The goodness of fit was great (McFadden's

pseudo-R2 of 0.6062 and 0.517 for the two stages F0 and FF, respectively).

The median dates, estimated from the model, for early flowering (F0) and late flowering (FF)

are shown in Table 3.

For the early flowering stage (stage F0) for the 2011 season, the estimated median date

occurred around April 11th (101.22 ± 0.80j) in Bellif, on April 6

th (96.5 ± 1.23 j) in Khroufa

and April 9th (99.27 ± 0.74) in Ain Snoussi (Table 4). There was no significant difference

between median dates for this stage in Bellif and Ain Snoussi (a lag of only 2 days). The

median date of this same stage was intermediary in Khroufa station. The lag between Bellif

and Khroufa was 5 days whereas between Khroufa and Ain Snoussi it was only 3 days.

The value of k rate, controlling the slope in the median, at stage F0 was dependent on the site,

however. The Ain Snoussi site had the highest k value (0.3723 ± 0.0499 trees / d) but was not

significantly different from Bellif (0.3302 ± 0.0287 tree / d). In contrast, that of Ain Snoussi

was the lowest (0.2262 ± 0.0191 tree / d), significantly different from the other two. Thus, the

majority of trees in Khroufa and Bellif took less time to reach stage F0, compared to those of

Ain Snoussi (Figure 6).



Figure 5: Kinetics into the start time (A) and end (B) of flowerings of Quercus suber L. for

the three study sites (Bellif, Khroufa, and Ain Snoussi) and adjusted logistic models.



Figure 6: Observed kinetics of cumulative leaf fall of Quercus suber L. for the three study

sites (A: Bellif, B: Khroufa, and C: Ain Snoussi) and the adjusted kinetic by the Bi-Richards

or Bi-logistics ( ) models and the increment of adjusted leaf fall ( ).



Table 3: Dates at the inflection point Ti (at which 50% of the trees have reached the stage in

question) of adjusted logistic models to evolution of the two onset stages (d1) and end of bud

break (d2) for the three study sites in 2010 and 2011. The values of the parameters that have

different letters are significantly different at a 0.05 level.

Table 4 :Dates at the inflection point Ti (at which 50% of the trees have reached the stage in

question) of adjusted logistic models to temporal evolution of the two onset stages (d1) and

end of bud break (d2) for the three study sites in 2010 and 2011. The values of the parameters

that have different letters are significantly different at a 0.05 level.

Site FO FF

Ti k Ti k

Bellif 101,22 ± 0,80a 0,35 ± 0,06a 125,09 ± 0,90b 0,2841 ± 0,05a

Khroufa 96,50± 1,23ab 0,24 ± 0,05a 122,57± 1,10b 0,2927 ± 0,05a

Ain Snoussi 99,27 ± 0,74a 0,38 ± 0,07a 136,42 ± 1,24a 0,1728 ± 0,02b

The flowering end date (stage FF) for the year 2011 took place on May 5 (125.09 ± 0.9j) in

Bellif, May 2 (122.57 ± 1.1j) in Khroufa and May 16 (136.42 ± 1.24j) in Ain Snoussi. Thus,

the earliest population was Khroufa and the last was Ain Snoussi. Moreover, there was no

difference between the Bellif and Khroufa stations but the difference was highly significant

(p <0.0001) between Ain Snoussi and the other two stations. The value of k rate (controlling

the slope in the median) at stage FF was only dependent on time. The Bellif and Khroufa sites

had the highest values of k (0.2841 ± 0.04808 tree/ day and 0.2927 ± 0.05722 tree/ day,

respectively), not significantly different from each other, however that of Ain Snoussi was

the lowest (0.1728 ± 0.02277 tree / day) and was significantly different from the other two.

Thus, the majority of trees in Khroufa and Bellif took less time to reach stage FF than those

of Ain Snoussi.

The flowering period (difference between the respective median dates F0 and FF) was 23.87

days in Bellif, 26.08 days in Khroufa and 72.96 days in Ain Snoussi. The flowering period

overlapped with the start and full bud dates. Indeed, flowering started with the beginning of

bud burst (range 0.3 j) in Ain Snoussi, just after the beginning of bud burst in Bellif and

Khroufa (differences of 7.82 days and 4.68 days, respectively) to extend and complete its

Site year d1 d2

Bellif : 2010 79,04 ± 0,75d 85,94 ± 0,65c

2011 93,38 ± 0,72a 108,27 ± 0,75a

Khroufa : 2010 83,30 ± 0,9c 90,56 ± 0,74d

2011 91,82 ± 0,96b 98,57 ± 0,88b

Ain Snoussi : 2010 97,67±0,71a 107,24 ± 0,91a

2011 98,97±0,70a 106,18 ± 0,87a



cycle after full bud stage (d2) from 16.82 days in Bellif, 23.93 days in Khroufa and 30.24

days in Ain Snoussi.

Therefore, we conclude that catkins developed concomitantly with the period of bud break,

completed their development earlier and fell after leaf expansion.

The onset of phenological events (early bud break and full bud, bloom) was not simultaneous

for all the trees and their duration was also different within the same station. Thus, for the

early stages and full bud, early and late flowering, intra-specific variability and very highly

significant differences were found (p <0.0001) at the three sites and over the two years of

observations. This inter-individual variability could be explained by changes in climatic

conditions.

Leaf fall: Leaf fall took place throughout the year, but generally for two phases with two

peaks, which varied according to the station and year. The quality adjustment was excellent

(Table 5) with errors often self-correlated (corrected using a covariance matrix of the type of

residue AR (n).

During the 2010 season for the Bellif station, the beginning and end of Phase 1 leaf fall of

Phase 1 were on February 13 (44.57 ± 2.49 days) and June 13 (estimated by the Bi-Richards

model), respectively, to reach a first peak around April 14, with a maximum speed of leaf fall

of 2.7733 ± 0.1023g / m² / day. This first phase lasted about 4 months. For the Khroufa

station, Phase 1 leaf fall started late, around April 13, reaching its peak around May 3 with a

maximum increase in leaf fall of 2.5611 ± 0.032 g / m² / day and ending around May 13. This

phase 1 lasted about one month, significantly lower than that of Bellif. In Ain Snoussi, leaf

fall began significantly later than Bellif and Khroufa. It occurred on May 2 and ended May 21

with a maximum daily increase of about 2.12 ± 0.4664 g / m² / day. The first peak was

reached on May 11. Its duration was very short compared to those of Bellif and Khroufa,

only 20 days.

During the same year of 2010, the beginning of Phase 2 leaf fall was earlier than that of phase

1 in the Khroufa and Ain Snoussi stations. It started about March 27 in Khroufa station and

February 26 in Ain Snoussi. However, in Bellif station, the start of phase 2 leaf fall took

place in the autumn, from October 10 to reach its peak about December 7 and be completed

in February of the following year. Thus, the length of leaf fall was almost 4 months. In the

other two stations, leaf fall ended around October 16 in Khroufa and on September 12 in Ain

Snoussi after a fall time of 203.2 days and 198 days, respectively in the three study stations,

maximum speeds of leaf fall during phase 2 were significantly lower than those of Phase 1.

They were recorded at 1.1595, 0.7859 and 0.7634 g / m² / day in Bellif, Khroufa and Ain

Snoussi stations, respectively.

Although leaf fall speed differed between the two phases, the K values (maximum relative

growth rate per unit of time) for both phases 1 and 2 remained relatively constant for Bellif

station. However, for both stations Ain Snoussi and Khroufa, the K value for Phase 2 was

significantly lower than that of Phase 1.



Table 5 Parameters (± SE) of the statistical model used (bi-Richards or bi-logistics) in order to model the cumulative falling leaves of cork oak during a

growing season, depending on the site and season. The derived quantities (±ES) from these parameters are presented here.

Bellif Khroufa Ain Snoussi

Models parameters 2010 2011 2010 2011 2010 2011

A1 302.98± 5.08 257.82±3.7519 49.2942±6.4397 80.622±9.39 24.76±6.24 142.18±1.9

t1i 104.59±1.4751 105.11±2.094 123.63±1.751 116.52±2.0789 131.63±3.27 123.36±1.1257

K1 0.009152±0.00043 0.01706±0.00133 0.0399±0.00681 0.0222 0.05784±0.02149 0.01466±0.00084

m1 2 3.0849±0.5312 3.3704±1.2315 2 2 2

A2 120.83±43.56 170.87±9.2723 146.33±7.785 90.49±8.57 134.74±5.85

t2i 340.91±19.51 345.7±3.2 173.33±8.63 188.28±11.8 156.62±3.77

K2 0.00958±0.0034 0.01948±0.00274 0.00537±0.00025 0.00517± 0.000554±0.00045

m2 2 7.8909±3.2878 1.6344±0.2382 2 2

Derived quantities :

Onset t10, phase 1 44.57±2.49 60.19±3.72 103.22±5.07 92.6167±2.8854 122.13±5.3449 85.88±2.0697

End t90, phase 1 164.61±3.74 128.77±3.17 133.06± 2.11 140.43±4.4664 141.13±4.20 160.84±2.7454

duration, phase 1 120.04±5.63 68.57± 4.85 29.83±5.66 47.81±6.26 18.9923±7.05 74.955 ± 4.309

increment. max., phase

1 2.77± 0.1023 4.40± 0.32 2.56 ± 0.20 2.13±0.15 2.1239±0.4664 2.0839 ± 0.1104

Onset t10, phase 2 283.57±8.5421 278.5±9.539 86.57±4.5334 82.11±10.57 57.394 ±5.857

End t90, phase 2 398.25±38.91 354.7±3.89 289.7± 8.0716 294.46±20.85 255.85 ±11.13

duration, phase 2 114.68±40.63 76.19±10.33 203.2±9.31 212.34±23.1504 198.45 ±16.10

increment. max., phase

2 1.1595±0.128 3.33±0.36 0.78 ±0.03234 0.4783±0.0759 0.7634 ±0.08097



During the year 2011 for Bellif station, the beginning and end of leaf fall estimated by the Bi-

Richards model during Phase 1 were on March 1 and May 8, respectively, to reach the first

peak around April 15, with a maximum leaf fall rate of about 4.4018 ± 0.3205 g / m² / day.

The estimated duration of the fall exceeded two months.

During the same 2011 season for Khroufa station, the beginning of Phase 2 leaf fall occurred

around March 23 and ended around October 16 after a fall time of about 212.34 days.

However, in Bellif station, Phase 2 leaf fall began in autumn, from October 5, to reach its

peak around December 12 and be finished about December 20; the duration of this phase was

almost 2½ months. For both stations Bellif and Khroufa, maximum speeds of of phase 2 leaf

fall (3.3277 and 0.4783 g / m² / day, respectively) were significantly lower than those of

Phase 1.

The values of K (slope at the inflection point) for both phase 1 and 2 remained constant for

the Bellif station. However, for Khroufa station, the value of K for Phase 2 was significantly

lower than that of Phase 1.

DISCUSSION

In a Mediterranean climate, the transition from winter to spring is characterized by an

increase in air temperature. There are thus the successive phases of budding leaf and flower

and leaf fall. However, the beginning of phenological events was not simultaneous for all

trees and duration was also different 21

.

Costae-Silva et al.23

also found that this species budding in the same period in Portugal.

However, Pinto et al.5 showed in their study of cork oak that the mean bud date was later,

between April and mid-May.

El Ennajah 28

, working on cork oak plants of different Tunisian provenances raised in a

nursery, also found that bud break occurred in late April.

The study sites varied by an altitudinal gradient, thus allowing us to follow the bud

phenology of Quercus suber L. over a fairly large temperature gradient over two years of

observations.

However, altitude and temperature are not always linearly correlated. Topography and

exposure might also have an additional effect on the temperature at a given site 2. This could

explain the absence of significant correlations between the median dates of bud burst and the

altitude or temperature.

The stages of beginning and full bud (d1 and d2) of Quercus suber L. were gradually lagged

with increasing altitude. This result is consistent with that obtained by Vitasse13

in different

species of the temperate region. This author has shown, the more the population of a species

is at a higher altitude, the later the average date of bud burst. He also showed that the average

bud break dates of two deciduous hardwood species (sessile oak and sycamore) are best

correlated with altitude; however, the houx (evergreen species) and beech have the least

correlated bud burst dates. Another study on deciduous and coniferous trees showed an

increase of 100 m altitude causes a two day delay in the date of bud burst 38

.

Overall, temperature explains phenological variations better than altitude whatever the

phenophase (bud, leaf senescence and the length of the growing season) and species13

.



The study of bud development kinetics helped highlight differences between the two years of

observation in the three stands of Quercus suber L. studied. The premature developing of

Quercus suber L. buds in 2010, remarkable at both stations Bellif and Khroufa, was related to

mild winter and spring temperatures. Indeed, an increase of more than 1°C (about 1.3 in

Bellif and 1.2°C in Khroufa) of the average air temperature in the period from January to

March could explain the lag beginning bud break of about 14 days in Bellif and 8 days in

Khroufa. This increase in temperature could also explain the lag in the full bud stage (d2)

from 22 days in Bellif to 8 days in Khroufa. However, an increase of 0.5°C in Ain Snoussi

apparently did not affect either the bud break start date or the full bud date. These results are

consistent with those observed in Quercus suber L in Portugal by Costae-Silva et al.23

; these

authors showing that an increase of 6°C in the air temperature caused an early budburst of 30

days. Another study also conducted on cork oak showed that a 1°C temperature in the spring

results in a 6-day precocity in bud break15

.

This same finding was observed in temperate deciduous and coniferous forests 13,38

. Several

studies of Mediterranean oaks have shown that air temperature is the main environmental

driver of budburst 5,15

. This high sensitivity of buds to changes in environmental conditions

reflects the phenological plasticity which plants have, especially in arid climates, to extend

the growing season before the summer drought 39

. Moreover, intra-specific models developed

by several researchers 40-44

on temperate, boreal and Mediterranean forests have also

demonstrated the central role of altitude and latitude in the phenological cycles and the

importance of the spring thermal regime (February to April) on phenology.

Although the cork oak population in Bellif accumulated the same amount of degree days over

the two years of observation, the beg bud date shifted 14 days, probably due to low

temperatures recorded in 2011 during the months of January and February. Thus it seems that

air temperature is the determining factor for the wood bud in this study area and for cork oak.

This result is consistent with those obtained by others researchers 5, 23, 45

. Similarly, Ogaya

and Penuelas14

in their study of Quercus suber phenology and floristic species showed that

Quercus suber buds depend on temperature whereas Arbutus unedo, Phillyrea latifolia buds

depend more on the availability of water.

However, for the site of Ain Snoussi, bud break occurred at almost the same period for both

seasons of observation 2010 and 2011, although the accumulated degree days were relatively

low (compared to other sites) and different for the two seasons (154 degree days in 2010 and

105 degree days in 2011); this was probably due to lower temperatures in 2011.

Furthermore, a sudden spring heat wave for a few days in the months before bud break

occurred in 2011. These lower cumulative temperatures in 2011 could also be due to base

temperature overestimation (8°C) in Ain Snoussi station since it is located more than 600 m

from the two other stations. Pinto et al.5 (2011) estimated base temperature at 6.2°C in

Quercus suber L., one very close to the temperature that triggers Quercus ilex L. buds and

needs about 323 degree days 15

.

Moreover, this base temperature varies depending on the station for the same species. It

would thus be better to estimate base temperature for each of the major biogeographic zones

of cork oak in Tunisia in order to estimate the heat requirements for bud break of this species.

As for Ain Snoussi, cork oak buds in Khroufa station also shifted one week without the

population having accumulated the same degree days. So aside from temperature, other

factors such as photoperiod and soil moisture are involved in this species' bud.



As for flowering, catkins developed concomitantly with the period of bud break and leaf

expansion and were widespread between mid-May and early June. Carita et al.46

showed that

the maximum flowering of Quercus suber L. in Spain takes place in June or July. These

authors also found that when conditions were favorable, there was a second period of

flowering. Quercus suber L. develops new leaves and catkins in the same period5. The same

phenomenon was observed in Quercus ilex L 14

. For Phillyrea latifolia L., flowering took

place in early spring when the leaves came out at the end of that season 14

(Ogaya and

Penuelas, 2004). However, Arbutus unedo L. developed new leaves in the spring while the

flowering took place in the autumn of the same year14

. These showed that flowering depends

on water availability.

Generally, floral development does not require environmental conditions as favorable as for

vegetative growth 47

. In Mediterranean regions, flowering occurs mainly in the spring 48

when

water is still available in the soil.

The variability of the phenological character observed between populations depends on two

factors: the intra-populational and inter populational variabilities, linked both to the effect of

the environment, but also to the genetic structure of the population 12, 13

.

In the three study sites, repeated measurements over time (2010 and 2011) of leaf fall showed

a fluctuating pattern: a period with a very large leaf fall which took place mainly in spring,

between April and May, succeeded by another period with low amounts of fallen leaves that

took place either in the autumn, between October and December or early summer (the whole

month of June or even July). This significant leaf fall spring is synchronized with the budding

trees. This same observation was made in Montpellier about oak 26

and in Portugal by

Oliveira et al.21

and Sa et al.49

. These authors showed that bud and leaf expansion occurred

either simultaneously or after the fall of old leaves. The latter continued until late spring.

However, in Spain, Caritat et al.50

showed that leaf fall took place in late spring, in May and

June, after budding and new leaves, like all Mediterranean oaks 50,51

(Andivia et al. 2012),

Milla et al.48

support the idea of Caritat et al.50

and showed that, among evergreen species,

leaf fall peaked just after vegetative growth (June, July) in spring (April, May). In studies

conducted on Quercus ilex L 52-54

2015) also showed that leaf fall of this evergreen species in

the Mediterranean has two peaks, the first occurring in spring just after budding and the

second in autumn (October-November).

The second two peaks observed in Ain Snoussi and Khroufa in early summer were explained

by Caritat et al. 46

and Caritat et al.50

by an adaptive strategy to water deficit that occurs

during this season following successive episodes of drought. This short period of abscission,

characteristic of Mediterranean forest ecosystems, takes place between June, July and August 21,46,50,

. Moreover, it should be noted that the life of the cork oak leaves in the sites observed

appeared to be short, not exceeding 12 months.

However, in Bellif the second peak occurred in autumn. Caritat et al.50

, Bussoti et al.54

;

Andivia et al.51,52

, in their studies of Quercus suber L. and Quercus ilex L., showed that this

second, smaller peak occurred when climatic conditions were favorable during the growing

season. This peak can be linked to the rhythmic growth of cork oak with the emission of a

wave of growth (flush) with the appearance of new leaves, which took place just after

summer and before air temperature fell50

. Thus, it would be interesting to conduct a fine

monitoring of the primary growth cork oak in the future and link the falling leaves to that.



Leaf fall fluctuated between stations and years. The highest fall rates varied from 2.77g m-

²day-1

to 4.4 g m-²day-1

in Bellif and from 2.56 to 2.13 g m-²day-1

in Khroufa. As for Ain

Snoussi, they were constant, approximately 2.1 gm-² day

-1. This same observation was made

about Scots pine in France and Douglas fir in Finland55

. Their growth rate ranged from 1.43

to 3.27 gm-² day

-1 in

Speulderbos for Pinus sylvestris and from 1.61 to 2.54 gm

-² day

-1 in

Hyytiala for Douglas fir. These fluctuations may be consequences that are due to irregular

weather conditions that can create high leaf loss or nutritional problems. The same

phenomenon was observed for Pins.

Since leaf fall rates varied from one year to another and from one station to another, it would

be interesting to carry out further subsequent studies to examine the causes of these

differences (nutrient cycles).

The use of statistical models (logistic model, Bi-Richards model which is the sum of two

Richards-Chapman models) made it possible to adjust the kinetics of the different

phenological phases (bud break, flowering and leaf fall) of Quercus suber L.

Different parameters characterizing this kinetics and derived quantities (start, end and

duration of phase) were defined thus making it possible to compare one station or one season

to another. Thus, the median date (early or full) of bud burst (beginning or ending), flowering

and the relative growth rate were estimated using a logistic model. The maximum speeds of

leaf fall, the maximum relative growth rate per unit of time, the dates of beginning and end of

leaf fall, and the length of each leaf falling phase were evaluated using the sum of two

Richards-Chapman models due to the two phases (superposed or sequential) of leaf fall. The

inflection time deducted from logistic models and Chapman-Richards corresponded to two

dates where leaf fall reached its peak (or maximum in terms of fall speed). In the future, it

would be interesting to generalize their use in further studies of plant phenology.

CONCLUSION

Geographical conditions, and therefore climate, are more important than species in deciding

phenophases. In Quercus suber, phenological stages seem to be well correlated with

temperature. This synchronization of phenophases corresponds to an adaptation of plant life

forms. Thus, the study of phenology requires special attention to climate variables and

particular events which might affect various phenophases.

The models used in this study could be used in phenological predictions for budding,

flowering and leaf fall of Quercus suber L., especially in Tunisia.

To detect the effects of climate change on the phenology of this species, a closer monitoring

in the future for a longer period of study will produce better results concerning budding,

flowering and leaf fall.

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