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Horticulturae 2024, 10, x. https://doi.org/10.3390/xxxxx www.mdpi.com/journal/horticulturae
Article 1
Description of Persian walnut (Juglans regia L.) phenological 2
events according to the extended BBCH scale 3
Julie Robin1, Anthony Bernard2, Lisa Albouy3, Sibylle Papillon3, Eloise Tranchand4, Marie-Neige Hebrard4, 4
Jean-Baptiste Philibert5, Marine Barbedette5, Sadia Schafleitner6, Bénédicte Wenden2, Teresa Barreneche2, Marine 5
Delmas6, Fabrice Lheureux7 and Julien Toillon1,* 6
1 Association Nationale des Producteurs de Noisettes (ANPN), 1500 Route de Monbahus, F-47290 Cancon, 7
France 8
2 INRAE, Univ. Bordeaux, UMR BFP, 71 Avenue Edouard Bourlaux, F-33882 Villenave d’Ornon, France 9
3 SCA Unicoque, Noisettes et Noix de France, 1500 Route de Monbahus, F-47290 Cancon, France 10
4 Station Expérimentale de Creysse, Perrical, F-46600 Creysse, France 11
5 Station Expérimentale Nucicole Rhône-Alpes (SENuRA), 385A Route de Saint Marcelin, F-38160 Chatte, 12
France 13
6 INRAE, Unité Expérimentale Arboricole, Domaine de la Tour de Rance, F-47320 Bourran, France 14
7 CTIFL, Centre Opérationnel de Lanxade, Prigonrieux, France 15
* Correspondence : jtoillon@anpn.eu (J.T.) 16
Abstract: Walnut trees are grown worldwide for their edible fruits of high nutritional value. To 17
address climate change, researchers have studied walnut phenology to create cultivars adapted to 18
warmer climates. The standardisation of walnut phenological observations is needed and the Bi-19
ologische Bundesanstalt, Bundessortenamt und CHemische Industrie (BBCH) scale is the most 20
accurate and internationally accepted for this purpose. Here, the principal growth stages (PGS) of 21
Persian walnut (Juglans regia L.) are described using stages from a previously available alphanu-22
merical scale. This standardised phenological scale describes Persian walnut growth from the 23
dormant vegetative state through reproductive budding to senescence. This phenological scale is 24
expected to increase the efficiency of walnut phenological monitoring. Fifty-seven stages were 25
used to describe the life cycle of Persian walnut in this BBCH scale. Of these 57 stages, 3 stages are 26
dedicated to seed germination (PGS-0), 4 stages to bud development (PGS-0), 7 stages to leaf de-27
velopment (PGS-1), 4 stages to stem elongation (PGS-3), 8 stages to inflorescence emergence 28
(PGS-5), 5 stages to male flowering (PGS-6), 5 stages to female flowering (PGS-6), 5 stages to fruit 29
development (PGS-7), 12 stages to fruit ripening (PGS-8) and 4 stages to leaf senescence (PGS-9). 30
Keywords: English walnut; phenology; phenophase; growth stages; climate change; global warm-31
warming 32
33
1. Introduction 34
Persian walnut (Juglans regia L.), also known as English walnut, is a widespread 35
tree of the Juglandaceae family. Juglandaceae comprises more than 50 species in 11 genera 36
such as Carya (hickories including pecans), Pterocarya (wingnuts) and Juglans (walnuts) 37
[1–3]. The Juglans genus includes more than 20 species, all of which are diploid (2n = 2x = 38
32), such as J. cinerea (white walnut), J. nigra (black walnut) and J. regia (Persian walnut) 39
[4–6]. Persian walnut is disseminated worldwide in temperate regions (Europe, North 40
and South America, South Africa, Asia, Australia and New Zealand), and was domesti-41
cated in central Asia (western Himalayas). It first spread to the west (northern Iran, the 42
Caucasus and eastern Türkiye) and then spread to the east (northern India and western 43
China) [7,8]. Persian walnut was present in refugia in the Balkans and western Europe 44
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Horticulturae 2024, 10, x FOR PEER REVIEW 2 of 15
during the last glacial period [9,10] and human-mediated dispersal is thought to have 45
occurred in the Early Bronze Age. 46
Persian walnut is a wind-pollinated, deciduous, monoecious and dichogamous tree; 47
its dichogamy limits self-fertilisation [2]. Usually, more than one hundred flowers form 48
the male catkin, whereas two or three flowers form the female inflorescence. 49
The study of the changes in the timing of seasonal events such as plant flowering is 50
called phenology [11]. There is a scientific consensus that phenology is dependent on 51
environmental conditions and impacted by climate change, as is the case for most de-52
ciduous tree species [12,13]. In Persian walnut, Charrier et al. [14] have shown that the 53
winter dormancy from September through January in the northern hemisphere is mainly 54
under environmental control. Climate change leads to phenological shifts that disrupt 55
the whole growth cycle of the trees. During the spring, a warming climate increases the 56
fulfilment of heat requirements and promotes earlier flowering and leaf unfolding 57
[15,16], making trees more susceptible to late frost. However, during the winter, a 58
warming climate counteracts phenological advancement because it decreases fulfilment 59
of chilling requirements [17,18]. Fu et al. [19] have shown that higher temperatures also 60
delay autumn leaf senescence, and the consequence of the phenological shift is the am-61
plification of drought stress because of the extended growing season [20]. 62
In Persian walnut, these phenological shifts have been observed in Slovenia [21] 63
and in Romania [22]; moreover Luedeling [23] has confirmed using partial least square 64
regression that the phenology of Persian walnut in California is advanced by high tem-65
peratures in spring and delayed by high temperatures in winter. Therefore, the phenol-66
ogy of dormancy in Persian walnut is impacted by both spring and winter temperatures, 67
which makes its response to climate change difficult to model [24–26]. For instance, fruit 68
winter chill modelling approaches are numerous and may perform poorly, so that the 69
quantification of chilling requirements may be imprecise [23,27]. 70
Differences in chilling and heat requirements are observable between genotypes of 71
a species: genotypes with low chilling requirements can flower earlier and may suffer 72
frost damages, whereas genotypes with high chilling requirements flower later and may 73
suffer insufficient chilling fulfilment, leading to abnormal growth and harvest loss [28–74
31]. In Persian walnut, a strong variability in chilling and heat requirement traits is ob-75
served in orchards and within herbarium accessions. In 2019 in France, Bernard et al. [32] 76
observed a 71-day gap in bud break date between the earliest and the latest accession in 77
the INRAE (Institut National de la Recherche Agronomique et Environnementale) wal-78
nut germplasm collection. In California, the germplasm collection of the Walnut Im-79
provement Program of the University of California-Davis showed a 44-day gap in the 80
leafing date in 2018-2019 [33]. This research has led to the identification of 81
SNP-phenological trait associations [33]. It is crucial to create a precise and globally ac-82
cepted scale of phenological observations in Persian walnut to ensure an efficient char-83
acterisation of genotypes whose data could be reused to feed models and statistical 84
analyses and to better manage orchards. 85
Based on a decimal code used in plant breeding by Zadoks et al. [34], the Biolo-86
gische Bundesanstalt, Bundessortenamt und CHemische Industrie (BBCH) scale was 87
first developed for cereal crops to help standardisation [35]. Later, Hack et al. [36] de-88
veloped an extended BBCH scale for other species such as pome and stone fruits. BBCH 89
scales are already available for other nut species, such as almond [37], cashew [38], 90
chestnut [39], hazelnut [40,41] and pecan [42]. However, a BBCH scale for Persian wal-91
nut is still missing. For Persian walnuts, a BBCH codification for flowering, fruit devel-92
opment and ripening stages only was recently presented during the IX International 93
Symposium on Walnut and Pecan organized by the International Society of Horticultur-94
al Science (ISHS) [43]. 95
To describe Persian walnut phenological events, Germain et al. [44] have released 96
the first scale that provides the basis for the International Plant Genetic Resources Insti-97
tute (IPGRI) descriptors of walnut phenology-related traits [45]. This scale has been used 98
Horticulturae 2024, 10, x FOR PEER REVIEW 3 of 15
by breeders and genetic resource curators across the world to characterise Persian wal-99
nut genotypes; for instance, the IPGRI scale has been used in Iran and India to describe 100
the phenological characteristics of promising genotypes [46–48]. Here, we propose an 101
extended BBCH scale for Persian walnut, adapted from the scales of Germain et al. and 102
IPGRI [44,45] and we provide pictures of the main stages useful for genotype character-103
isation. We expect this work to contribute to meeting findable, accessible, interoperable 104
and reusable (FAIR) data principles and to contribute to better genetic resource man-105
agement and crop practices. 106
2. Materials and Methods 107
2.1. Study area 108
The phenological phases of Persian walnut were monitored in a varietal collection 109
orchard composed of 10 cultivars (Table 1) and located in Agmé (59 m above sea level, 110
N44.495210, E0.357202) in southwestern France in the department of Lot-et-Garonne. 111
The trees are 11 years old. The soil type is a clay loam (20.5% sand, 41.4% silt and 38.1% 112
clay). This soil has a pH of 8.3, an organic matter content of 1.8 g · kg-1 and a C/N ratio of 113
9.2. 114
Table 1. List of cultivars planted in the varietal collection orchard. 115
Cultivar name
Reference
Franquette
[2]
Ferbel
[3]
Lara
[2]
Livermore
[49]
Forde
[50]
Gillet
[51]
Durham
[52]
Tulare
[53]
Howard
[54]
Chandler
[54]
116
2.2. Monitoring of phenophases and fruit growth measurements 117
The phenological stages of flowering and leaf development were monitored weekly 118
from April to September on 16 trees per cultivar. These observations were repeated in 119
2019, 2020, 2021, 2022 and 2023. 120
Fruit development was monitored weekly from early May to late August 2022 on 40 121
fruits on trees of the ‘Lara’ cv. Fruits were randomly chosen in the orchard. On each 122
fruit, the length (from the basal scar to the apical scar) and the width were measured 123
with an electronic calliper (MarCal 16 EWRi digital calliper IP66). Then the fruits were 124
weighed with a precision balance (Mettler Toledo model MS-S/MS-L). Means (n = 40) are 125
presented with their standard deviations. For lignification, the method described by Pa-126
radinas et al. [40] was used. 127
2.3. BBCH scale characteristics 128
The development of Persian walnut was described using main growth stages num-129
bered from 0 to 9 according to the extended BBCH reference scale [36]. The numerical 130
order of the main growth stages was respected in the first digit of this scale. The second 131
digit of this scale describes the plant or organ stage in further detail. To avoid errors 132
during phenology monitoring, male flowering was described using a two-digit code 133
while female flowering was described using a three-digit code. As for hazelnuts [40], 134
once the walnut husk and the shell were fully developed, a third digit was added to de-135
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scribe kernel development. For fruit development, a third digit was added to the 136
two-digit scale of fruit ripening to detail the percentage of falling fruits at maturity. 137
138
3. Results 139
All the stages presented in this section are described in Table 2 and illustrated in 140
Figure 1. 141
3.1. Principal growth stage 0: seed germination 142
The principal growth stage 0 for seed germination is subdivided into 3 develop-143
mental stages and presented with three-digit codes to avoid ambiguity between seed 144
germination and bud development, which is expressed with a two-digit code. 145
Stage 000, which corresponds to stage 89 of fruit ripening in this scale, represents 146
the dry seed. When the radicle emerges from the seed, stage 050 is reached. Finally, 147
stage 090 represents the beginning of root growth when the rootlet elongates, absorbent 148
hairs appear and secondary root development begins, and the shoot emerges from the 149
seed and pierces the soil surface. 150
3.2. Principal growth stage 0: bud development 151
The principal growth stage 0 for bud development is subdivided into 4 develop-152
mental stages. Bud development stage 00, which was ‘Af’ in the Germain scale is 153
reached when buds are dormant and covered by scales. When the hard scales of the first 154
order fall and buds are still enveloped by poorly differentiated semi-membranous scales, 155
stage 03 is reached, historically described as stage Af2. Once the bud swells (stage Bf), 156
the outer envelopes loosen and the ends of the underlying bracts covered with whitish 157
down appear. This is the so-called ‘woolly’ or ‘white bud’ stage described in this scale as 158
stage 07. The final stage, initially described as stage Cf, represents bud elongation, when 159
the extremity of the outermost leaves can be distinguished, also known as bud burst. 160
Here, bud burst is described as stage 09. 161
3.3. Principal growth stage 1: leaf development 162
The principal growth stage 1 for leaf development is subdivided into 7 develop-163
mental stages. Historically, 3 stages were used to describe leaf development. Stage Cf2, 164
which represents the separation of the scales and bracts and the beginning of separation 165
of the first leaf, is here described as stage 10. When the bud is open, the first leaves are 166
separated and their leaflets are well individualised, stage 11 is reached, initially de-167
scribed as stage Df. Finally, stage 12 represents the point at which the first leaves are 168
completely unfolded and erect and have taken on an oblique habit, revealing the female 169
flower in their centre. Four new stages are here added to the historical description. These 170
are stage 13, which represents the point at which the first leaf is fully developed with a 171
loss of red colour, stage 14, representing the point at which more than two leaves are 172
fully developed with a green colour, stage 17, corresponding to the point at which all the 173
leaves are fully expanded and have a dark-green colour and stage 19, which represents 174
the complete development of leaves on the tree. 175
3.4. Principal growth stage 3: stem elongation 176
The principal growth stage 3 for stem elongation is subdivided into 4 developmen-177
tal stages. The beginning of stem elongation is described as stage 30. This stage is 178
reached when the stem has elongated to less than 10% of its final length. Stage 31 is 179
reached when the stem has elongated to between 10% and 50% of its final length. When 180
the stem has elongated to between 50% and 90% of its final length, stage 35 is reached. 181
Finally, when the stem has elongated to more than 90% of its final length, stage 39 is 182
reached. 183
184
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185
Figure 1. The phenological growth stages of Persian walnut according to the BBCH codification. 186
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187
188
Figure 1. The phenological growth stages of Persian walnut according to the BBCH codification. 189
190
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Table 2. Description of BBCH stages applied for Persian walnut. 191
BBCH
codification
Germain et al.,
1999 scale
IPGRI scale
Description
Principal growth stage 0: seed germination
000
Dry seed
050
The radicle emerges from the seed
090
Rootlet elongation, appearance of absorbent hairs and secondary
root development, and soil emergence of the beetle
Principal growth stage 0: bud development
00
Af
Dormant buds: scale-covered bud
03
Af2
Fall of the hard scales of the first order. Bud still enveloped by other
poorly differentiated semi-membranous scales
07
Bf
The bud swells: the outer envelopes loosen, and the ends of the
underlying bracts covered with a whitish down appear this is the
so-called "woolly" or "white bud" stage.
09
Cf
The bud elongates; the extremity of the terminal leaves of the
outermost leaves can be distinguished; it's the bud burst
Principal growth stage 1: leaf development
10
Cf2
The scales and bracts move apart, the first leaves begin to separate
11
Df
The bud is open, the first leaves separate, and their leaflets are well
individualised
12
Df2
The first leaves are completely unfolded, first erect, then they take
on a more or less oblique habit, revealing the female flowers in their
centre.
13
First leaf fully developed, loss of red foliage colour
15
More than two leaves are fully developed with a green foliage
17
All the leaves are fully expanded, are growing and turn dark green
19
All the leaves are mature and have their final length
Principal growth stage 3: stem elongation
30
Starting stem elongation
31
<10% of final stem length
33
>10% and <50% of final stem length
35
>50% and <90% of final stem length
39
>90% of final stem length
Principal growth stage 5: inflorescence emergence
50
Amr
In early summer, the differentiated male catkin, globose in shape,
has a pinkish hue while the buds remain green
51
Amv
During the summer, the catkin grows slightly, becomes conical,
reaches about 0.5 cm length, and takes on a green colour
53
Amg
At the beginning of October, the catkin stops growing, it measures
0.5-0.8 cm and takes on a gray colour that it will keep all winter.
55
Bm
About 3 weeks before the bud break, growth resumes, the catkin
swells and lengthens to reach 1.3-2 cm length
57
Cm
Catkin, stiff and oblique, reaches the size of a pencil and measures
3-4 cm. Its colour gradually changes from green-brown to light
green; the flower clusters are distinct.
58
Dm
Catkin loses its rigidity, becomes semi-drooping; the glomeruli
separate
59
Dm2
The glomeruli space out and begin to open; the catkin hangs
590
Ef
Appearance of female flowers
Principal growth stage 6: flowering
60
Em
First male bloom date
Complete opening of the glomeruli and separation of the anthers
which begin to turn yellow
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61
Fm
Peak male bloom date
Beginning of anther dehiscence from base of catkin
65
Fm2
Peak male bloom date
Complete anther dehiscence, full pollen emission
67
Gm
Last male bloom date
The anthers emptied of their pollen turn black
69
Hm
The catkin falls to the ground and dries up
610
Ff
First female bloom date
Appearance of stigmata
630
Ff1
Peak female bloom date
The orange-yellow stigmata are divergent. Their receptivity is opti-
mal: it is the full female flowering.
650
FF2
Peak female bloom date
Stigmata take on a pale green-yellow colour and are completely
recurved
670
FF3
Last female bloom date
The stigmata begin to become necrotic; these are streaked with fine
brown threads.
690
Gf
Drying and blackening of the stigmata
Principal growth stage 7: fruit development
71
Beginning of fruit-husk growth
75
50% of the final size in fruit husk
79
100% of the final size in husk and beginning of lignification: begin-
ning of resistance to the knife
790
100% of the shell is lignified and the beginning of kernel filling
799
100% lignified shell and kernel filling completed
Principal growth stage 8: fruit ripening
81
White septum in kernel
82
Beginning of browning with some brown pitting on the septum
83
Brown internal septum on 1/3 of its surface
84
Packing tissue brown date
Brown internal septum on 3/3 of its surface
85
In allover brown septum but damp and matt
86
Shiny dry brown septum
87
Cracking of the husk
88
Opening of the husk: the nut remains trapped in the husk
89
Husk opens enough for the nut to freely fall to the ground
891
Harvest date
< 10% of the nuts have fallen to the ground
895
Harvest date
> 50% of the nuts have fallen to the ground
899
Harvest date
100% of the nuts have fallen to the ground
Principal growth stage 9: leaf senescence
93
Beginning of leaf colour change
95
50% of the leaves have changed colour
97
All the leaves have changed colour and leaf fall begins
99
Defoliation date
All the leaves have fallen
192
3.5. Principal growth stage 5: inflorescence emergence 193
The principal growth stage 5 for inflorescence emergence is subdivided into 7 de-194
velopmental stages for male inflorescence emergence and 1 stage for female inflo-195
rescence emergence. These stages are an adaptation of the Germain et al. and IPGRI scale 196
into the BBCH codes. The first stage (stage 50), initially described as stage Amr, occurs in 197
early summer. The differentiated male catkin, globose in shape, has a pinkish hue while 198
the buds remain green. Then, during the summer, the catkin grows slightly, becomes 199
conical, reaches about 0.5 cm in length, takes on a green colour and reaches stage 51 200
(Amv). Stage 53 occurs at the beginning of October, when the catkin stops growing, 201
measures 0.5–0.8 cm in length and takes on a grey colour that will be kept during the 202
winter. About 3 weeks before bud break, growth resumes, the catkin swells and length-203
ens to reach 1.3–2 cm in length and reaches stage 55 (Bm). When the catkin remains stiff 204
and oblique, reaches the length of a pencil and measures 3–4 cm, stage 57 is reached 205
(Cm). Its colour gradually changes from green-brown to light green and the flower clus-206
ters become distinct. Stage 58 (Dm) is reached when the catkin loses its rigidity, becomes 207
Horticulturae 2024, 10, x FOR PEER REVIEW 9 of 15
semi-drooping and the glomeruli separate. When the glomeruli spread out and begin to 208
open, the catkin hangs and reaches stage 59 (Dm2). 209
The appearance of the first female flowers is here described as stage 590. Generally, 210
this stage occurs just after stage 12, when the first leaf is completely unfolded. This stage 211
was historically named Ef. 212
3.6. Principal growth stage 6: flowering 213
As Persian walnut develops male and female reproductive organs on separate 214
flowers, two codifications of developmental stages are here developed, a two-digit code 215
for male flowering and a three-digit code for female flowering. 216
3.6.1. Male flowering 217
The principal growth stage 6 for male flowering is subdivided into 5 developmental 218
stages. The first male bloom, historically named Em, is described here as stage 60 and 219
represents the complete opening of the glomeruli and separation of the anthers, which 220
begin to turn yellow. When male blooming peaks, the dehiscence of anthers begins from 221
the base of the catkin. This stage is stage 61 (Fm). Stage 65 represents full pollen emis-222
sion and complete anther dehiscence, initially described as Fm2. When the anthers that 223
are emptied of their pollen turn black, stage 67 is reached. Stage 67 is also known as the 224
late male bloom date or Gm. Finally, when the catkin falls to the ground and dries up, 225
stage 69 is reached (Hm). 226
3.6.2. Female flowering 227
The principal growth stage 6 for female flowering is subdivided into 5 develop-228
mental stages. The appearance of stigmata, initially described as stage Ff or ‘first female 229
bloom date,’ is described here as stage 610. When the orange-yellow stigmata are diver-230
gent, their receptivity is optimal: this stage is known as full female flowering. Full fe-231
male flowering was previously described as stage Ff1 and is here described as stage 630. 232
The next stage, here described as stage 650, occurs when stigmata take on a pale 233
green-yellow colour and are completely recurved (Ff2). When the stigmata begin to be-234
come necrotic, they are streaked with fine brown threads and stage 670 is reached (Ff3). 235
This stage is known as the last female bloom date. The last stage of female flowering, 236
stage 690, occurs when the stigmata dry and blacken (Gf). 237
3.7. Principal growth stage 7: fruit development 238
The principal growth stage 7 for fruit development is subdivided into 5 develop-239
mental stages. The beginning of fruit husk growth is here described as stage 71. When 240
the fruit husk has reached 50% of its final size, stage 75 is reached. Complete growth, 241
that is, when the fruit husk has reached 100% of its final size and lignification begins, 242
manifested by a low resistance to the knife when the nut is cut, is here described as stage 243
79. When 100% of the shell is lignified and the kernel begins to fill, stage 790 is reached. 244
When kernel filling is complete, stage 799 is reached. Persian walnut fruit development 245
is illustrated in Figure 2. Fruit size (length and width) and weight change over time fol-246
low similar curves. These growth curves can be divided into two phases, a first phase 247
that represents rapid fruit husk and shell growth between BBCH stages 71 to 79 and a 248
second phase with slower fruit growth, during which the kernel grows, between BBCH 249
stages 790 to 799. 250
3.8. Principal growth stage 8: fruit ripening 251
The principal growth stage 8 for fruit ripening is subdivided into 12 developmental 252
stages. The first stage, here described as stage 81, is reached when the white septum is 253
observable. When the septum begins to brown and develops some brown pitting, stage 254
82 is reached. Stage 83 occurs when one-third of the internal septum is brown. When the 255
entire surface of the internal septum is brown, stage 84 is reached. This stage is known 256
as the septum browning date. Stage 85 describes the point at which the septum is com-257
pletely brown but still damp and matte. When the septum is shiny, dry and brown, stage 258
Horticulturae 2024, 10, x FOR PEER REVIEW 10 of 15
86 is reached. Then, when the husk cracks, stage 87 is reached. The next stage, 88, is 259
reached when the husk begins to open but the nuts remain trapped in the husk. When 260
nuts fall freely to the ground, stage 89 occurs. This stage can also be described as stage 261
000 if the BBCH code for seed germination is used. 262
The harvest date is subdivided into three stages: stage 891, which represents the 263
point at which fewer than 10% of the nuts have fallen to the ground, stage 895, the point 264
at which more than 50% of the nuts have fallen to the ground and stage 899, the point at 265
which 100% of the nuts have fallen to the ground. 266
267
268
Figure 2. Nut growth dynamic of nut length (black line ), width (dash line ) 269
and weight (dash-point line ) of ‘Lara’ cultivar associated with their standard de-270
viation of mean. 271
272
3.9. Principal growth stage 9: leaf senescence 273
The principal growth stage 9 for leaf senescence is subdivided into 4 developmental 274
stages. Stage 93 occurs when leaf colour change begins. When more than 50% of the 275
leaves have changed colour, stage 95 is reached. Stage 97 is reached when all the leaves 276
have changed colour and leaf fall begins. Finally, when all the leaves have fallen, the 277
defoliation date is reached, here described as stage 99. 278
4. Discussion 279
The Persian walnut BBCH scale that is outlined in this paper uses 9 principal 280
growth stages and 57 detailed stages to describe the developmental phenophases of Per-281
sian walnut. This level of detail is in agreement with other BBCH scales of nut tree fruits 282
that have been developed, such as the scale for hazelnut with 53 stages [41], chestnut 283
with 48 stages [39], almond with 39 stages [37] and pecan with 51 stages [42]. The BBCH 284
scale outlined in Table 2 allows walnut phenological monitoring data that have been 285
recorded in one of the three historically used scales to be translated into BBCH codes. 286
4.1. Flowering phenophases 287
To develop a strictly numerical scale, male flowering is here presented using a 288
two-digit code and female flowering is presented using a three-digit code using the 289
same method that has previously been used for hazelnuts [40,41]. This method has the 290
advantage of preventing confusion between male and female flowering because Persian 291
walnut can be protogynous, protandrous or homogamous depending on the cultivar. 292
4.2. Fruit development 293
Horticulturae 2024, 10, x FOR PEER REVIEW 11 of 15
Development of the fruit, that is, the nut, is described using an outline view. Fruit 294
development is divided into two steps. The first step, concerning husk development, is 295
described by stages 71 to 79 in this scale and the second step, concerning shell develop-296
ment and lignification, is described by stages 790 to 799. Kernel development and rip-297
ening are described using stages 81 to 89. Nut fall is detailed using three-digit codes 298
from the beginning of fall (stage 891) to the point at which all nuts have fallen to the 299
ground (stage 899). Nut growth shows a sigmoidal curve, with a rapid growth phase 300
from May to mid-June, a slowdown in growth from mid-June to late June and finally a 301
halt in growth in the beginning of July. The nut weight shows a slight increase of 5 g 302
during fruit ripening from the gelatinous phase of the kernel (stage 79) to the time the 303
nut is dry and rich in lipids and proteins (stage 899) [56]. 304
4.3. Orchard and research implications of BBCH codification 305
The BBCH scale that is outlined here will allow the standardisation of phenological 306
stage description between research teams and advisors. The use of numerical stages will 307
simplify the use of phenological stages in models using phenological characteristics. In 308
commercial orchards, the application of phytosanitary products is generally recom-309
mended for a specific BBCH stage that has not been described for Persian walnut before 310
2023. Indeed, the first communication presenting a BBCH scale for Persian walnuts was 311
presented by Papillon et al. during the XI International Symposium on Walnut & Pecan 312
in June 2023 hosted by the ISHS [43]. 313
5. Conclusions 314
The scale described here is the first to detail Persian walnut phenophases in 57 315
stages from seed germination to leaf fall. The two-digit and three-digit codes used for 316
presenting male and female flowering provides an advantage to avoid ambiguity during 317
phenology monitoring. Finally, the use of strictly numerical codes provides an ad-318
vantage when data are stored in computer files, including tables. This proposed pheno-319
logical scale is expected to increase the efficiency of both worldwide germplasm charac-320
terisation and breeding and provide help for future comprehensive studies of the adap-321
tation of Persian walnuts to climate change. 322
323
Author Contributions: Conceptualization, J.T.; methodology, J.T, J.R, S.P.; validation, J.R., A.B., 324
L.A., S.P., E.T., M-N.H., J-B.P., M.B., S.S., B.W., T.B., M.D., F.L. and J.T.; formal analysis, J.T. and 325
L.A.; investigation, J.T, J.R, S.P. and L.A.; resources, J.T.; data curation, J.T. and L.A.; writ-326
ing—original draft preparation, J.R., A.B. and J.T.; writing—review and editing, A.B. and J.T.; su-327
pervision, J.T.; project administration, J.T. All authors have read and agreed to the published ver-328
sion of the manuscript.” 329
Funding: This research received no external funding. 330
Data Availability Statement: The data presented in this study are available on request from the 331
corresponding author. The data are not publicly available due to auto financial support of the 332
members of the French National Association of Hazelnut Growers (ANPN) and the cooperative 333
Unicoque. 334
Acknowledgments: The authors thank the technical staffs of the Association Nationale des Pro-335
ducteurs de Noisettes (ANPN), Station Expérimentale de Creysse, Station Expérimentale Nucicole 336
Rhône-Alpe (SENuRA), Centre Technique Interprofessionnel des Fruits et Légumes (CTIFL), IN-337
RAE, and of the cooperative Unicoque Noisette et Noix de France. The authors specifically grate-338
ful Charlène Thiriet for the providing of some pictures illustrated the scale. The authors thank the 339
editor and the reviewers for their useful comments on the manuscript. 340
Conflicts of Interest: The authors declare no conflicts of interest. 341
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