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Annals of Applied Biology ISSN 0003-4746
RESEARCH ARTICLE
Phenological growth stages of cacao plants (Theobroma sp.):
codification and description according to the BBCH scale
N. Niemenak1,2,C.Cilas
3,C.Rohsius
2,H.Bleiholder
4,U.Meier
5&R.Lieberei
2
1 Department of Biological Science, Higher Teachers’ Training College, University of Yaounde I, P.O. Box 47 Yaounde, Cameroon
2 Department of Crop Science and Plant Ecology, University of Hamburg, 22609 Ohnhorststrasse 18, Hamburg, Germany
3 CIRAD Avenue Agropolis, TA A31/02, 34398 Montpellier, France
4 Dinkelackerring 4, 67435 Neustadt, Germany
5J¨
ulius K ¨
uhn-Institut, Institut f ¨
ur Kulturpflanzenforschung, Messeweg 11/12, D 38104 Braunschweig, Germany
Keywords
BBCH scale; growth stages; phenological
development; Theobroma cacao.
Correspondence
Dr Nicolas Niemenak, Department of
Biological Science, Higher Teachers’ Training
College, University of Yaounde I, P.O. Box 47
Yaounde, Cameroon.
Email: niemenak@yahoo.com
Received: 26 June 2008; revised version
accepted: 29 June 2009.
doi:10.1111/j.1744-7348.2009.00356.x
Abstract
The detailed description of growth stages of useful plants followed by adequate
codification facilitates communication between scientists and practicians if,
for example, new findings of science have to be transferred to management
procedures or if experiences made at one growing site have to be adapted
to another. We describe the growth stages of the worldwide species of
cacao trees (Theobroma sp.) to prepare the basis for production management,
comparisons of epidemiological studies of disease, of growth patterns under
different environmental factors and of genetically clone specific parameters. The
codification follows the ‘extended BBCH (BBCH, Biologische Bundesantalt,
Bundessortenamt and CHemische Industrie, Germany) scale’, a numerical
system that differentiates between principal, secondary and tertiary growth
stages. Each growth stage presented from seed germination to crown
development and harvest is correlated with general management practices.
This scale will be of great help to cacao growers and scientists around the world
for better communication, more efficient planning of management practices
and experiments.
Introduction
The cacao plant is a neotropical, small, evergreen
tree native to South America (Motamayor et al., 2002)
growing between 20◦latitude north and south of the
Equator. Since its discovery by Europeans after the
conquest of the New World, its cultivation has developed
strongly since its introduction into Africa. The first
attempt to plant cacao outside the American continent is
attributed to the introduction of a plant from Mexico into
the Philippines in 1670 (Blanco, 1837). In West Africa the
first material was introduced in 1822 through S˜ao Tom´e
and Pr´
ıncipe and was from ‘lower’ Amazonian origin
(Bartley, 2005).
This plant, of the Malvaceae (formerly Sterculiaceae)
family, is grown for its fruits, known as cacao pods.
Botanically the fruits are berries. The pods contain seeds,
which are fermented with the mucilage surrounding them
and then dried to give fermented dried cacao, the raw
material used to make chocolate. The cacao tree is a
small tree whose fruits grow on both the trunk and the
branches. The fruits arise from the pollination of flowers
grouped in flower cushions. A distinction is currently
made between three major groups of cultivated cacao
trees: ‘Criollo’, ‘Forastero’ and ‘Trinitario’ (Cheesman,
1944; Bartley, 2005).
Several systems have been proposed to describe the
phenological growth of cacao tree (Vogel, 1975), but
no unified approach in describing phenological stages of
growth that are compatible with other plant species has
been defined for this species. Growth stage definitions
for other plants have been developed by several groups.
An interdisciplinary working group proposed a uniform
decimal code to describe phenological growth stages of
Ann Appl Biol 156 (2010) 13 –24 ©2009 The Authors 13
Journal compilation ©2009 Association of Applied Biologists
Growth stages of cacao trees are described on the basis of the ‘extended BBCH scale’ N. Niemenak et al.
crops and weeds (Lancashire et al., 1991; Hack et al.,
1992). The BBCH scale provides a uniform decimal code
to describe the phenology of plants like cereals, maize,
citrus, stone and pome fruits, coffee, roses and others.
Reviews have been published by Meier (1997) and Meier
et al. (2009).
In our work, we proposed to apply the BBCH system
to describe the phenological growth stages of the cacao
tree, from germination up to tree senescence (Hack
et al., 1992). The BBCH scale describes the pattern of
development independent of variation in timing. The
basic principles of the scale integrated: (a) morphological
characteristics which are used for the description of
the phenological developmental stages; (b) the same
code is applied for similar phenological stages of each
plant species; (c) for each code, a description is given,
and for some important stages, drawings are included;
(d) development of the main stem is manly taken
into consideration; (e) relative values relating to species
and/or variety-specific ultimate sizes are used for the
indication of sizes (Hack et al., 1992).
Material and methods
To describe the phenological growth stages of cacao plant,
the extended BBCH scale will be used. The BBCH scale
(Bleiholder et al., 1991) and the extended BBCH scale
(Hack et al., 1992) consider 10 principal growth stages
(‘macro stages’) numbered from 0 to 9 and each macro
stage considers 10 secondary growth stages numbered
from 0 to 9. The combination gives a two-digit numeric
code.
For T. cacao, these begin with the germination of seeds
or budding establishment (BBCH 0). The vegetative and
generative growth is considered under eight principal
growth stages corresponding to leaf development on
the main shoot of the young plant and on the fan
branches (BBCH 1); main stem elongation, formation
of a jorquette with its fan branches and, subsequently,
chupon initiation and chupon growth (BBCH 2); fan
branch elongation (BBCH 3); inflorescence emergence
(BBCH 5) and flowering (BBCH 6). Development of fruit
(BBCH 7), ripening of fruit and seed (BBCH 8) and
senescence (BBCH 9) complete the scale.
When cacao plants are in the juvenile stage of
development, their structure and growth characteristics
are easier to observe, and measurements are made
with greater accuracy than is possible in the case of
adult trees. The intrinsic characteristics of older trees
are often indiscernible owing to the alterations to their
architecture and canopy form that result from external
factors (Bartley, 2005). In cultivated fields, particularly,
pruning and harvesting practices and competition create
significant changes in tree structure. Therefore, during
our description, we will put more emphasis on the
juvenile stages. Identification of differences between
cacao plants with regards to vegetative development in
the early stages of juvenile growth is usually scanty.
The specific BBCH scale for cacao plant is based on a
decimal code of at least two digits and a description of the
individual developmental steps. In the present paper the
scale for cacao plant is presented in two forms.
Two-digit code
The first digit describes the principal growth stage (0– 9)
and describes 10 clearly recognisable and distinguishable
more long-lasting developmental phases. The second digit
describes the secondary stage (0–9) or points of time or
steps of plant development. In contrast to the principal
growth stages, they are defined as short developmental
steps characteristic of the cacao plant.
Three-digit code
The two-digit code is not precise enough in all
developmental steps to describe a specific step. Therefore
in this case a third digit is introduced between the
principal growth stage and the secondary growth stage.
The so-called mesostage gives the flexibility to provide
a further subdivision of the secondary growth stages, if
necessary. The scale is then built by three digits, where:
•the first digit indicates the principal growth stage
(0–9),
•the second digit the mesostage (0 – 9),
•the third digit the secondary growth stage (0–9).
Results and discussion
Principal growth stage 0: germination–vegetative
propagation
Cacao fruit reaches physiological maturity around
150 days after flowering and is harvested at 170 days.
After harvest, seeds are removed from the fruit and
are processed to obtain raw cacao by fermentation
and drying. They die in the course of this treatment.
Under permissive conditions (Fig. 1a) they germinate.
The period from onset of imbibition to seedling emergence
takes approximately 25 days. Imbibition is completed
within 3 days and radicle protrusion appears around day
5 (BBCH 02). Radicle and hypocotyl elongation proceeds,
hypocotyl is visible (BBCH 03) and the formation of
root hairs follows (BBCH 05). Between days 7 and 18,
depending on the conditions, seedlings have emerged
from the soil (emergence) and the hypocotyl forms a hook
14 Ann Appl Biol 156 (2010) 13 – 24 ©2009 The Authors
Journal compilation ©2009 Association of Applied Biologists
N. Niemenak et al.Growth stages of cacao trees are described on the basis of the ‘extended BBCH scale’
(3–5 cm long) lifting the cotyledons from the ground
(BBCH 07, Fig. 1b and Fig. 1c); the cotyledons are upright
but still closed (BBCH 09) (Hunter, 1959; Rohsius, 2000).
Different forms of vegetative propagation can be applied
to cacao such as budding and somatic embryogenesis
(Miller & Guiltinan, 2003). However, the planting
materials found in the field come mainly from seeds
and are improperly called ‘clonal seeds’ (seeds obtained
from a number of trees of a single clone planted in
isolation or from a mixture of several clones), most
of which are derived from open-pollinated pods taken
from the same tree clones. Budding is performed with
softwood stem-cuttings either from plagiotropic (fans)
or orthotropic material (chupons). Initiation of budding
from orthotropic or fan shoots is characterised by the
emergence of root through the cortical tissues just above
the callus (Cheesman, 1944). Somatic embryos, when
established display the same growth behaviour as seeds
(Maximova et al., 2002; Niemenak et al., 2008).
Based on orthotropic materials, stage 00 encompassed
stem cuttings with four or five leaves taken from the
nursery trees, with their leaves trimmed to about half of
their normal size. Stage BBCH 01 represented cuttings
with their cut end dipped in a solution of naphthalene
acetic acid (0.5%) and β-indole-butyric acid (0.5%) and
then put in a rooting medium. Callus formation and root
emergence are considered as stage BBCH 02.
Initiation of horizontal growth of tap roots constitutes
the stage BBCH 03 whereas the switch from horizontal
to vertical growth is the stage BBCH 05. The break and
growth into a vertical leading shoot of terminal or lateral
buds from orthotropic cuttings marked the stages BBCH
07 and BBCH 09, respectively (Charrier, 1969).
Principal growth stage 1: leaf development on the
main shoot of the young plant and on the fan branches
Leaf development on upright shoots (main stem or
chupon) as well as on the jorquette is considered. Instead
of a regular sequence of successive leaves expanding
in cacao, about 10 leaves start to grow at the same
time, which is referred to as a leaf-flush (Greenwood
& Posnette, 1950; Greathouse et al., 1971). They expand
almost simultaneously, and an interval of approximately
40 days intervenes before a new leaf-flush occurs again.
The flush cycle shows a typical pattern: leaf unfolding
(F-1), expansion (F-2), maximum leaf area and greening
(I-1) and maturity (I-2) (Greathouse et al., 1971; Sleigh
et al., 1984). The leaves, throughout expansion, are pale
green or tinged with pink depending on the presence
or absence of anthocyanins (Holden, 1957). They are
soft and delicate, but gradually harden. Red pigmented
leaves also become green during hardening. The new
leaves attain their full size in the course of about 4
weeks after unfolding. The successive flushes can be
easily distinguished by the degree of browning of the
stem on which the leaves are attached. Young flushes
display green stems whereas the oldest flushes appear on
dark brown stem.
Leaves show dimorphic characters corresponding to the
stem on which they arise. On the upright shoot, leaves
have long petioles and are symmetrical; the petioles have
a marked pulvinus or swelling at each end which allows
the leaf to be oriented in relation to the light. The leaves
on the fan-wood have shorter petioles and are slightly
asymmetrical. Also the vigour and general size of the
chupon leaves are usually greater than in leaves of the
fan branches. The leaf blades are simple, lanceolate to
lanceolate-ovate. The margin is entire and slightly wavy.
The venation is pinnate, and the surface is glabrous on
both sides (Brooks & Guard, 1952; Vogel, 1975).
The development of the first leaves (eophylls) from
seeds begins after the cotyledons start to unfold (BBCH
10, Fig. 1d). The subsequent leaves occur as a succession
of flushes. Each flush emerging from the main shoot or
from a fan branch is counted up to the 9th flush and
assigned BBCH codes 11 to 19, respectively.
The BBCH stage 110 is attributed to the emerging of
unfolded leaves of the first flush, which are still pale
green or red depending on the cultivar. When leaves
expand and display 20% or 50% of their final size,
BBCH stage 112 (Fig. 1e) or 115 is reached. The mature,
flush–bearing, already hardened leaves with dark green
colour and constant size are classified as BBCH stage 119
(Fig. 1f).
Principal growth stage 2: main stem elongation,
formation of jorquette of fan branches and chupon
An individual shoot passes through alternate periods of
growth and dormancy. The growth period is characterised
by the expansion and the elongation of leaves of the
shoot. During dormancy the length of the shoot remains
constant, and no new leaves expand. Shoot-growth
rhythm is correlated to the flush cycle and therefore
displays the same patterns, that is bud swelling (F-1),
stem elongation (F-2), maximum stem size (I-1) and
maturity (I-2) (Greathouse et al., 1971; Sleigh et al., 1984).
Maturation phase is achieved when the stem bearing the
newly formed leaves begins to form phloem. In this
phase, the stem is brown, the leaves are mature and the
stipules covering the terminal bud are more or less closely
appressedtoit.
Shoot derived from seedling (BBCH 20) has a deter-
minate orthotropic growth. Later this shoot constitutes
the main trunk. After 1–2 years of growth, the shoot
Ann Appl Biol 156 (2010) 13 – 24 ©2009 The Authors 15
Journal compilation ©2009 Association of Applied Biologists
Growth stages of cacao trees are described on the basis of the ‘extended BBCH scale’ N. Niemenak et al.
1a BBCH 00 1b BBCH 07 1c BBCH 08
1d BBCH 10 1e BBCH 12
1f BBCH 19/20
Figure 1 Principal growth stages of cacao plant 0 and 1.
16 Ann Appl Biol 156 (2010) 13 – 24 ©2009 The Authors
Journal compilation ©2009 Association of Applied Biologists
N. Niemenak et al.Growth stages of cacao trees are described on the basis of the ‘extended BBCH scale’
reaches the physiological maturity and the apical meris-
tem stops growth (BBCH 209). Branch dimorphism is
then induced and a jorquette of plagiotropic branches is
developed (BBCH 21, Fig. 2a and Fig. 2b). The height at
which the first jorquette is produced depends on environ-
mental conditions, such as light, soil fertility, the age of
a plant at establishment in the field and on the genotype
(Vogel, 1975).
A second vertical stem growth (first chupon) appears
on the main stem by the activation of the orthotropic
buds in the leaf axils below the whorl of lateral branches
(BBCH 211). In the course of time a second whorl of fan
branches is developed (BBCH 22, Fig. 2c). This process
may be repeated several times (BBCH 29) when there is
no competition from other vegetation and no pruning.
This mode of development is a characteristic of growth
architectural model found in tropical rain forest known
as Nozeran model (Hall ´eet al., 1978). As a consequence,
the canopy becomes higher. In a cacao plantation, trees
will grow to a height of 4– 10 m depending on spacing,
the degree of shade and the frequency of pruning. In
the wild, under the heavy shade of the primary forest
they reach a height of up to 20 m (Wood & Lass, 1985;
Bartley, 2005).
Principal growth stage 3: fan branch elongation
A young cacao seedling produces a single vertical
unbranched stem. When it attains physiological maturity,
the terminal bud gives rise to jorquette of three, four
or five fan branches which grow out obliquely to
horizontally depending on the genotype and conditions.
Branch elongation is devoted only to the jorquette which
is considered as the primary fan branch. Fan branches
branch, and their auxiliary buds produce shoots; that is
fan branches of the second or higher orders (Greathouse
et al., 1971; Greenwood & Posnette, 1950).
According to the BBCH scale, when an individual fan
branch produces 20 secondary fan branches stage 32 is
applied (Fig. 2d). The 30th, 40th or more secondary fan
branch is described accordingly with BBCH 33, 34, till 39.
Principal growth stage 5: inflorescence emergence
Cacao is cauliflorous, with flowers growing on the main
trunk and branches. An individual flower cushion bears
flowers at different stages of development (Fig. 3a).
Cacao flowering is usually abundant with up to 120 000
flowers per tree each year. Flowering occurs mainly
between January and June in West Africa and Brazil
(Mossu et al., 1981; Paulin et al., 1983; Valle et al., 1990).
Lower-Amazon Amelonado genotypes stop flowering
from July to November (Mossu et al., 1981), whereas
upper-Amazon genotypes usually produce flowers
throughout the year. In all cases, flowering intensity
decreases with increasing number of developing pods
per tree because of the competition for assimilates (Valle
et al., 1990).
In T. cacao, flower development has been characterised
using morphological and anatomical landmarks (Bayer
& Hope, 1990; Swanson, 2005). Development of an
individual flower encompasses 12 stages and takes
30 days. Stages 1 – 6 involve meristem development
and the organogenesis of the floral organs, which is
completed within 10 days. Stages 7 – 12 imply the process
of elongation and differentiation of the individual organs
up to the fully developed flower (Bayer & Hope, 1990;
Swanson, 2005).
The BBCH scale does not describe the timing and
micro events of inflorescence. Only the macro events
are considered. The development of a flower bud on
a leaf scar (young plant) or on flower cushions (tree) is
coded by BBCH stages 51 –59. BBCH stage 51 is defined by
the emergence of flower primordium (Fig. 3a). Buds are
approximately 150 μm long and visible. From BBCH stage
52 to 56, buds expand with subsequent sepals (BBCH 55)
and pedicle growth (BBCH 56). At BBCH 55, sepals are
relatively thick and display half of the total thickness
of the developing flower (Swanson, 2005). Through
elongation, the outside of the flower bud changes colour
from green to white or reddish. At stage 59 flower buds
are mature with an average length of 6 mm, an average
width of 4 mm and a pedicle measuring about 14 mm.
Buds are still closed.
Principal growth stage 6: flowering
When a bud matures, the sepal tissues form a series
of five longitudinal abscission zones from the tip to the
base of the floral bud. These longitudinal abscission zones
separate, forming the five individual sepals which then
expand and open outwards. As the sepals open outwards,
the petals open at the same time. The opening of flowers
occurs over a 12-hour period. Sepals split during the
afternoon and continue to open during the night. Early
the following morning, the flowers are fully open and the
anthers release their pollen (Swanson, 2005).
Flower opening is very well synchronised between
the cohorts of mature flowers opening each night. The
flowers open at almost exactly the same time and rate,
irrespective of their position on the trunk. Unfertilised
flowers abscise from the trunk approximately 1 day after
flower opening (Cheesman, 1932). This is completed just
prior to opening of the next set of flowers, and results
in increased visitation of pollinators to the newly opened
flowers by the reduction in competition of the day-old
flowers.
Ann Appl Biol 156 (2010) 13 – 24 ©2009 The Authors 17
Journal compilation ©2009 Association of Applied Biologists
Growth stages of cacao trees are described on the basis of the ‘extended BBCH scale’ N. Niemenak et al.
2a BBCH 21/201
2b BBCH 21/219,
Ch1 : first chupon
•Ch1
2c BBCH 22/23,
Ch1: first chupon,
Ch2: second chupon,
Jb:Jorquett of fan
branches
•Ch1
•Ch2
•Jb
2d BBCH 31/32
Figure 2 Principal growth stages of cacao plant 2 and 3.
When about 10% of the flowers on a plant are open,
stage 61 is achieved. At stage 65, about 50% of the flowers
have opened. At stage 69 about 90% of the flowers have
opened (Fig. 3a and Fig. 3b).
Principal growth stage 7: development of fruit
After anthesis the growth and maturation process of the
cacao fruit, which is approximately 150 days, falls into
two phases (McKelvie, 1956).
The first phase is a developmental phase, occupying
about 75 days during which the pericarp enlarges in
conjunction with the ovules (BBCH 71, Fig. 3c and
Fig. 3d). Endosperm cellularises and both dry and fresh
weight of the pulp increase exponentially. This phase
also comprises two periods. The first of these covers
an interval of about 50 days during which the zygote is
dormant (Cheesman, 1927). Growth in length is slow. The
second period (50–75 days) of the first phase commences
with the division of the zygote and the preliminary
development of the embryo. Fruits begin to swell up
and their length also increases. At the end of the first
phase, the ratio between the diameter and the length
of an individual fruit is about 0.35. Fruits are called
cherelles and display about 50% of their final size (BBCH
75, Fig. 3e).
During this phase, fruits are susceptible to physi-
ological deterioration named ‘cherelle wilt’. Cherelle
wilt is the shrivelling and blackening of young cacao
fruit, which accounts for a considerable loss of fruits
(Humphries, 1943a,b).
The second phase (BBCH 77, Fig. 3f and Fig. 1g), which
starts about 85 days after pollination, is a period of active
18 Ann Appl Biol 156 (2010) 13 – 24 ©2009 The Authors
Journal compilation ©2009 Association of Applied Biologists
N. Niemenak et al.Growth stages of cacao trees are described on the basis of the ‘extended BBCH scale’
3a BBCH 51-55/60-61
52
61
60
•55
•51
3b BBCH 59/60-61
59
61
60
3c BBCH 70 3d BBCH 71 3e BBCH 75
3f BBCH 77 3
g
BBCH 78/81
Figure 3 Principal growth stages of cacao plant 5 –8.
metabolism, during which lipids, storage proteins and
anthocyanins accumulate in the seed while the moisture
content of the embryo decreases up to 30% (Lehrian &
Keeney, 1980; Pence, 1991). Pericarp and ovule growth
slows down at the expense of embryo growth. The embryo
grows from 0.2 cm in length after 85 days to over 3 cm
after 150 days. At this stage it completely fills the inner
space, which is confined by the measures of the testa of
the seed. Before embryo growth becomes rapid, the ovule
becomes filled with a jelly like endosperm. When embryo
Ann Appl Biol 156 (2010) 13 – 24 ©2009 The Authors 19
Journal compilation ©2009 Association of Applied Biologists
Growth stages of cacao trees are described on the basis of the ‘extended BBCH scale’ N. Niemenak et al.
growth ceases, there is no further resumption of fruit
growth and ripening begins immediately (BBCH 79).
Principal growth 8: ripening of fruit and seed
The increase of the external dimensions of fruit
ceases 150 days after fertilisation; at that time the
embryos are almost fully grown. Fruit and seed have
reached their physiological maturity and ripening follows
immediately. It takes about 20– 30 days to complete,
and its characteristic is that the colour of the husk
changes externally. Green pods become orange-yellow
and red coloured pods turn into orange pods or stay
red. Fruit colour increases its intensity with green/yellow
or red/orange areas (BBCH 85). Internally, at the seed
level, the cells of the hypodermal layer of the outer
integument, and some of the adjacent layers beneath,
become prismatic in shape and highly mucilaginous, their
walls ultimately disappearing, so that the ripe seed is
surrounded by a continuous sheath of mucilage.
Altogether, the maturation process of the fruit, from
the pollination to fully mature fruit, takes 160 – 210 days
(Berry & Cilas, 1994). The mature fruit of cacao is an
indehiscent drupe that remains attached to the tree by
its peduncle until harvested, distributed by animals or
until deteriorated on the trunk. The husk of the fruit is
woody and is of varying thickness according to variety.
According to the five loculi in the superior ovary (the
number of ovules per ovary is clone dependent and varies
between 37 and 65), the seeds are arranged in five rows
in the fruit. The number of seeds per fruit range usually
between 20 and 50. The cotyledons of the seeds are more
or less convoluted and their colour varies from white
to dark purple depending on the genotype combination
after fertilisation.
Principal growth 9: senescence
The physiological life of a cacao tree can reach ages of
more than 100 years because the tree can regenerate itself
by the production of chupons. However, the economic
life of a cacao field is influenced by the environmental
conditions. The highest cacao yields are achieved between
25 and 40 years (Tafani, 1977).
Leaves on an individual flush have a determinate life
time. The longevity of leaves of adult trees of cacao
with closely packed crowns varies with their position
within the canopy, and/or the irradiance received, and
the time of emergence. In particular, longevity decreased
greatly with the height of the leaf from ground level
(Miyaji et al., 1997). Where conditions are accordingly,
the leaves remain for three or four flushes. When the
development of an individual flush is completed, the
leaves are dark green and are of normal size (BBCH
90). After 4–5 months of maximum activity, senescence
phase is initiated: the leaf changes its colour from green
to yellowish (BBCH 92). This process is accompanied and
finished by the formation of an abscission layer at the base
of the basal pulvinus (BBCH 95). Post harvest treatments
(fermentation and drying) or storage are included in
BBCH 99.
Conclusion
The BBCH scale allows the description of cacao growth
process and a comparison with other cultivated species.
As the system exploits the presence or absence of distinct
morphological criteria, it can be used to determine
stage of growth in an objective, unequivocal manner
so that communication of cacao research results and
producer practices can be facilitated. This may also allow
identifying the scarcity in the knowledge of the growth
process in cacao. For example, the duration of different
steps of cacao growth and development are not well
characterised. In addition, the model can act as a stepping
stone for constructing future mechanistic models, with
the aim of better understanding cacao development in
genetic, physiological, ecological, evolutionary terms as
well as quality purpose. Application of mineral fertiliser
is one of the most important measures in agricultural
plant production whereby accuracy in distribution will
influence success both in cultivation and economy. This
study will help cacao culture by expressing the timing of
agricultural operations on a standardised scale.
Phenological growth stages and extended BBCH-identification keys of cacao plant
Principal growth stage 0: seed germination/vegetative propagation
Code
Two-digit Three-digit Description
00 000 Fresh seeds /Orthotropic cuttings with four or five half-trimmed leaves
01 001 Seed imbibition/Cuttings planted in rooting media; no callus visible
02 Radicle protrusion through the seed coat/Callus formation begins on orthotropic cuttings; tap root
emergence
20 Ann Appl Biol 156 (2010) 13 – 24 ©2009 The Authors
Journal compilation ©2009 Association of Applied Biologists
N. Niemenak et al.Growth stages of cacao trees are described on the basis of the ‘extended BBCH scale’
Continued
03 Hypocotyl visible; elongation of radicle/Initiation of horizontal growth of tap roots
05 First side roots visible/Vertical orientation of tap root growth
07 Hypocotyl forms a hook; cotyledon emergence from the ground/Terminal or lateral buds from
orthotropic cuttings break
09 009 Elongation of the hypocotyl completed; cotyledons are upright, but still unfolded/Growth of terminal or
lateral buds into a vertical leading shoot
Principal growth stage 1: leaf development on the main shoot of the young plant and on the fan branches
Code
Two-digit Three-digit Description
10 100 Cotyledon completely unfolded
Stipules surrounding terminal bud on the main shoot or fan branches spread apart and bud swells
11 110 Leaf unfolding on the first flush. Leaves are pale green or red
111 Leaf expansion is 10% of final size
112 Leaf expansion is 20% of final size
115 Leaf expansion is 50% of final size
119 First flush growth complete. Leaves are dark green with maximum area
12 120 Leaf unfolding on the second flush. Leaves are pale green to red
121 Leaf expansion is 10% of final size
122 Leaf expansion is 20% of final size
125 Leaf expansion is 50% of final size
129 Second flush growth complete
19 190 Nine or more flushes completely mature
Principal growth stage 2: main stem elongation, formation of jorquette of fan branches and chupon
Code
Two-digit Three-digit Description
20 200 Shoot derived from seedling displays 10% of growth
202 Shoot with 20% growth
203 Shoot with 30% growth
205 Shoot with 50% growth
209 Shoot reaches its physiological maturity and the growth of its apical meristem is arrested
21 210 Formation of the first jorquette and subsequently the first chupon
211 First chupon appears under the first jorquette with 10% growth
212 First chupon with 20% growth
215 First chupon with 50% growth
219 First chupon reaches its physiological maturity and the growth of its apical meristem is arrested
22 220 Formation of second jorquette and subsequently the second chupon
221 Second chupon appears under the first jorquette with 10% growth
222 Second chupon with 20% growth
223 Second chupon with 50% growth
229 Second chupon reaches its physiological maturity and the growth of its apical meristem is arrested
23 230 Formation of third jorquette and subsequently the third chupon
231 Third chupon appears under the third jorquette with 10% growth
232 Third chupon with 20% growth
233 Third chupon with 50% growth
239 Third chupon reaches its physiological maturity and the growth of its apical meristem is arrested
29 290 Formation of ninth or more jorquette and subsequently ninth or more chupon
291 Ninth or more chupon appears under the ninth jorquette with 10% growth
292 Ninth or more chupon with 20% growth
293 Ninth or more chupon with 30% growth
295 Ninth or more chupon with 50% growth
299 Last chupon reaches its physiological maturity and the growth of its apical meristem is arrested
Ann Appl Biol 156 (2010) 13 – 24 ©2009 The Authors 21
Journal compilation ©2009 Association of Applied Biologists
Growth stages of cacao trees are described on the basis of the ‘extended BBCH scale’ N. Niemenak et al.
Principalgrowthstage3:fanbranchelongation
Code
Two-digit Three-digit Description
31 301 Jorquette of primary fan branches visible
32 302 Primary fan branch with 20 secondary fan branches
35 305 Primary fan branch with 50 secondary fan branches
39 309 Primary fan branch with 90 or more secondary fan branches
Principal growth stage 5: inflorescence emergence
Code
Two-digit Three-digit Description
51 501 Flower buds visible (buds primordium 150 μmwide)
52 502 Flower buds expanded, emergence of sepal primordia (bud <1 mm long)
55 505 Flower buds expanded, sepals enclose bud (bud 1– 2 mm long)
56 506 Flower bud expanded, emergence of pedicle (bud 2– 3 mm long)
58 508 Flower bud expanded, bud turning from green to white (bud 2– 4 mm long)
59 509 Flower bud growth complete (buds 6 mm long and 3 mm large; pedicle 14 mm), buds still closed
Principal growth stage 6: flowering
Code
Two-digit Three-digit Description
60 600 First flowers getting open
61 601 Beginning of flowering
62 602 10% of flowers open
65 605 50% of flowers open
69 609 90% of flowers open
Principal growth stage 7: development of fruit
Code
Two-digit Three-digit Description
70 700 Fruits at the main stem or branches visible
71 701 Beginning of fruit growth. Endosperm cellularisation, ovule and pericarp development. Beginning of the cherelle
wilt phase. Fruits have reached 10% of final size (zygote dormant)
72 702 Division of the zygote and preliminary development of the embryo. Fruits swell. Fruits have reached 20% of the
final size
75 705 End of the cherelle wilt phase. D/L 0.35. Fruits have reached 50% of the final size
76 706 Beginning of the non-wilting phase. Ovule filled with jelly like endosperm. Fruits have reached 60% of the final size
77 706 Fat, storage proteins and anthocyanins accumulated in the cotyledons. Endosperm is gradually resorbed by the
embryo. Fruits have reached 70% of final size
79 709 Embryos are full-grown, only traces of endosperm remain round the fleshy cotyledons. Increase in the external
dimension of fruit ceases. Fruits have reached 90% of the final size
Principal growth stage 8: ripening of fruit and seed
Code
Two-digit Three-digit Description
81 801 Change of fruit colour from green or red to yellow or orange
85 805 Increase in fruit colour intensity
89 809 Fruit is fully ripe, attached to the main stem or branches and can be harvested with knife or cutlass
22 Ann Appl Biol 156 (2010) 13 – 24 ©2009 The Authors
Journal compilation ©2009 Association of Applied Biologists
N. Niemenak et al.Growth stages of cacao trees are described on the basis of the ‘extended BBCH scale’
Principal growth stage 9: senescence
Code
Two-digit Three-digit Description
90 900 Flush completed its development, leaves appear dark green
92 902 Older leaves begin to discolour from dark green to yellow
95 905 Formation of abscission zone in the basal pulvinus of the old leaves
98 908 Abscission of old leaves
99 909 Post harvest or storage treatments
Acknowledgements
The study was supported by the Alexander von Hum-
boldt Stiftung (www.humboldt-stiftung.de) via grant to
Niemenak Nicolas (Grant No KAM/1115305). We thank
Olivier SENE (Department of Plant Biology, Faculty of
Science, University of Yaounde I) for drawings.
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