Ann. uppl. B i d .

(1997), 130:135-140
Printed in Great Britain 135

Phenological stages of the pomegranate tree (Punica

granatum L.)
B~ P MELGAREJO, R MARTINEZ-VALERO, J M GUILLAMON, M MIRO
and A AMOROS
Plant Production Department, Universidad Polite'cnica de Valencia, Ctra. de
Beniel km. 3 '2, Orihuela (Alicante), Spain
(Accepted 28 November 1996)

Summary
As in other temperate species, the pomegranate tree shows different
phenological characteristics through its vegetative cycle in response to changing
temperature. This phenology has been studied as a basis for comparisons of the
successive stages of growth and reproduction in different geographical areas and
conditions. The variety Mollar de Elche was studied, since it is grown on more
than 95% of the total area devoted to this crop in Spain. Thirteen phenological-
stages were identified during the annual cycle, starting at bud in dormancy and
finishing a year later with leaf fall. These stages are denoted using the BBCH
General Scale which uses numerical codes to represent particular stages. The code
uses a two-digit number to describe the different phenological states and makes it
possible to distinguish between principal and secondary stages of development.
The duration of stages was measured in days and as accumulated degree-day.

Key words: Phenological stages, pomegranate tree

Introduction
The pomegranate tree (Punica granatum L.) originates in central near east (Sanchez-
Monge, 1974). It is a temperate species that is now cultivated throughout the Mediterranean
region. It requires high summer temperatures to ripen properly so commercial production is
limited to coastal areas or those with mild summers (Melgarejo & Martinez, 1989). It can be
grown in areas where the winter temperatures drop to -15°C and certain acidic and central
Asian cultivars can even survive temperatures of -25°C or -30°C (Aleksandrov, 1950).
The plant's needs during winter are small (Westwood, 1982), and the length of winter
dormancy is correlated with temperatures below 16°C (Rozanov & Vorobeva, 1976).
Fleckinger (1945) first studied phenological stages of fruit trees such as pear and apple and
represented them graphically. In this scheme the stages of vegetative development of shoots
and branches, the thickening of branches and trunk, and the later appearance of flowers and
fruit and their subsequent development were defined by descriptions of their external
appearance, and each denominated on individual phenological stage (Gil-Albert, 1991).
Bleiholder, van den Boom, Langeluddeke & Stauss (1989) introduced a new nomenclature
which described the phenological stages of both herbaceous and woody plants. The new
system, BBCH General Scale, unified previous codes which were specific to different
botanical families into a general scale applicable to all plants. Stauss (1994) published a more
detailed version of this scale. The new method is basically a decimal system which identifies
01997 Association of Applied Biologists
136 P MELGAREJO ET AL.

different development stages by a two digit code. The first digit defines its major stages using
values of 0 to 9 while the second digit, also scaled 0 to 9, relates to secondary stages.
The nomenclature has already been used by various authors for different plant families:
Zadoks, Chang & Konzak (1974) for cereals; Lancashire et al. (1991) for rape, bean and
sunflower: Meier et al. (1 993) for beet; Hack et al. (1993) for potato; Meier et al. ( I 994) for
fruit with stones and pips, redcurrant and strawberry; Lorenz ef al. (1994) for vine; Feller ef
ul. (1995) for several vegetables, and Agusti ef al. (1995) for citrus species. Until now their
has been no study of the phenological stages of pomegranate.
This paper describes the phenological stages of pomegranate using the traditional nomen-
clature described by Fleckinger (1945) and other authors for fruit trees, and relates them to the
BRCH General Scale.

Materials and Methods

’The pomegranate trees used were of the variety “Mollar de Elche” (Melgarejo, 1993). the
most widely grown variety in Spain. They were grown on a plantation belonging to the
Polytechnic University of Valencia which lies within the municipal boundaries of Alicante.
The trees were produced by vegetative propagation, planted in a 4 m x 3 m pattern. and
watered by a system of drip irrigation.
The soil was a clay loam, typical of the region. Rainfall is scarce (about 300mm per
annum), the majority falling in spring and autumn. Mean annual temperature was 19°C with
mild winters and hot summers (1 1°C in January and 28°C in August). According to the
agroclimatic classification of Papadakis (Anon., 1986) the climate is subtropical
mediterranean, and ideal for pomegranate cultivation.
The different phenological stages of plant growth and bud and fruit development between
winter dormancy and leaf fall were defined and described using the traditional procedure of
Fleckinger (1 945) in which the general stages are designated by letters followed by a number
between 1 and 4 to designate the substage. Two consecutive stages should be sufficiently
c h e in time for a bud’s evolution to be clearly identified. These stages were related to the
BBCH General Scale.
Four healthy trees were chosen at random within the plantation and four branches growing
toward each of the four cardinal compass points marked. The development of a single bud on
cach branch was monitored closely. In addition, all trees in the plantation were inspected to
ascertain the predominant growth stage at each visit (every 2 to 4 days until June and then
once per week). Photographic records were taken every 2 wk. Measurements and observations
were made between December 1991 and December 1992, at which time all the leaves had
fallen and the trees were entering their period of winter dormancy. Shoot, flowers and fruit
growth W ~ measured
E during the growth cycle with a Cassio electronic digital gauge (accurate
to within 0.01 mm).

Results
l h e growth stages, the phenological codes and duration are given in Table I and also in Fig.
I.
The pattern of development of individual buds of marked trees generally matched that of
ihc wholc plantation even though flowering was dependant on the position and orientation of
the branches on the tree. There was no appreciable difference between buds for the duration of
the succeshive phenological stages.
 Phenological stages of the pomegranate tree 137

Table 1. Growth stages, phenological codes and duration of the pomegranate tree
Growth stage Fleckinger code BBCH code Duration days Duration "C days
Bud in winter dormancy A 00 61 -
Bud swelling B 01 11 12
Red tip C 09 6 25
Sprouting of first leaves D 10 6 21
Leaf separation D2 10 4 20
Leaf growth D3 11 12 44
Lengthening of internodes D4 31 119 1228
Appearance of the flower buds E 51 3 21
Swollen calyx E2 55 11 88
Opening of calyx E3 59 3 24
Open flower F 61 6 59
Petals fall G 67 2 27
Fruit setting H 69 10 129
Young fruit I 71 17 182
Fruit growth J 73 90 1323
Second bud sprouting K 39 45 700
Fruit ripening L 81, 85 35 366
Leaf fall M 93 57 -

The duration of each phenological stage was measured in days and heat units starting at the
beginning of bud development. The heat units were measured as the sum of the differences
between mean daily temperatures and a base temperature of 10°C which corresponds to the
temperature at which bud development is activated (Baldini, 1992). The use of heat units
allows comparisons to be made across different years and geographical areas.

Phenological stages of development

A: 00: Bud in winter dormancy

The bud is greyish brown and completely closed, deeply linked to the twig and sharply
pointed at its tip.

B: 01: Bud swelling

The bud swells and becomes paler and rounder in shape.

C: 09: Red tip

The bud opens to show the new shoot, which is spear shaped and has a red tip.

D: 10: Sprouting of the first leaves

The first leaves appear; they are furled and are bright red with a pale midrib green and the
rest of the leaf is bright red.

02: 10: Leaf separation

The new leaves separate.
138 P MELGAREJO ET AL.

D3: 1I : Leaf growth

Leaves grow in length and width, and change colour from bright red to light green.

D4: 31: Lengthening of internodes

Internodes lengthen and shoot growth is rapid.

E: 51: Appearance of the flower buds

Flower buds appear among the leaves on shoots, being greenish at first, but becoming red
after a few days. The sepals are visible and close together.

E2: 55: Swollen calyx

The buds increase in size, and become pear-shaped; the differences between male and
hermaphrodite flowers becomes apparent in the shape and the colour of the calyx: the terminal
branches bud together with several flowers, usually abscises.

E3: 59: Opening qf the calyx

The sepals open, to show the folded red petals inside. Toward the end of this stage, petals
unfold and the pistil anthers become visible.

F. 61: oyen floLver

The calyx opens totally and the protruding petals, which are folded and purple, unfold over
the sepals. The petals seem to be inserted between every two sepals, on their inner side, giving
the impression of alternating petals and sepals. The anthers of the stamen change to deep
yellow when the pollen is ripe and capable of fertilising. It is during this stage that pollination
takes place.

G: 67: Petal fall

Petals wither and fall; the calyx turns colour from red to orange-red; stamens bend toward
the longitudinal axis of the flower and the anthers become greyish-yellow. The terminal part
of the style withers.

H: 69: Fruit setting

‘The fertilised ovary grows in size and the base of the calyx swells; the stamens wither and
the fruit slam changes from orange-red to greenish brown.

I : 71: Young ,fruit

The fruit increases in size rapidly and the colour turns from greenish brown to green.

J: 7.3: Fruit growth

The frwt enlarges almost to its final size through cell enlargement; the sepals fonn a crown,
thc dry stamen being inside.

K: 39: Second bud sprouting

Resumption of shoot growth on the tree.
 Phenological stages of the pomegranate tree 139

L: 81, 85: Fruit ripening

The fleshy seeds change from white to pinkish-red or red; the skin of the fruit changes from
green to greenish yellow, and finally to brownish-yellow with reddish patches.

M: 93: Leaf fall

The leaves turn yellowish, and fall; and when complete, winter dormancy starts.

Acknowledgements
The authors thank M I Mir6 for help with the English translation and D Antonio Campos for
the drawings which accompany the text.

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(Received 29 January 1996)