Annals of Botany 103: 1325– 1336, 2009

doi:10.1093/aob/mcp079, available online at www.aob.oxfordjournals.org

Is axis position within tree architecture a determinant of axis morphology,

branching, flowering and fruiting? An essay in mango
Frédéric Normand1,*, Abdoul Kowir Pambo Bello1,†, Catherine Trottier2 and Pierre-Éric Lauri3
1
CIRAD, UPR HortSys, Station de Bassin-Plat, BP 180, 97455 Saint-Pierre Cedex, Reunion Island, France, 2Université
Montpellier II, UMR I3M, #5149, Équipe ‘Probabilités et Statistique’, 34095 Montpellier Cedex 5, France and 3INRA, UMR
DAP, #1098, Equipe AFEF, 2 place P. Viala, 34060 Montpellier Cedex 1, France

Received: 12 January 2009 Returned for revision: 10 February 2009 Accepted: 6 March 2009 Published electronically: 5 April 2009

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† Background and Aims Growth and reproductive strategies of plants are often related to particular, although
usually poorly characterized, spatial distributions of shoots within the plant’s architecture. In this study it is
therefore hypothesized that a close relationship exists between architectural position, axis morphology (length,
diameter, leaf area), and functional behaviour (branching, flowering and fruiting). The study focused on the archi-
tectural position of mango growth units, defined here as being the relative position, apical or lateral, on the parent
growth unit, i.e. growing from the apical or a lateral meristem, respectively.
† Methods Stem length and leaf characteristics (area, dry weight) were measured on apical and lateral growth
units of four mango cultivars over two years. Branching, flowering and fruiting were assessed for both growth
unit types using an exhaustive description of tree vegetative and reproductive growth over two years. The
relationships between growth unit diameter and flowering and fruiting were assessed for one of the four cultivars.
† Key Results A pronounced morphological dimorphism was observed for the four cultivars. Across cultivars,
stem length was significantly 1.31 –1.34 times longer and total leaf area was 2.54– 3.47 times larger in apical
compared to lateral growth units. Apical growth units tended to branch, flower and fruit more than lateral
growth units. The relationship between growth unit diameter and flowering rate was quadratic and dependent
on growth unit position. The relationship between growth unit diameter and fruiting rate was linear and indepen-
dent of growth unit position.
† Conclusions Morphological traits of mango growth units were clearly involved in the determinism of flowering
and fruiting, although in different ways. The results, however, showed that current hypotheses of flowering, such
as carbohydrate availability and florigenic promoters, are not sufficient in themselves if they neglect the
hierarchical relationships between axes, i.e. their relative position, apical or lateral.

Key words: Axis dimorphism, branching, flowering, fruiting, growth unit, Mangifera indica, mango, Reunion
Island.

IN T RO DU C T IO N the adaptive behaviour of plants faced with evolutionary con-

straints. For example, in dioecious species, different reproduc-
Growth and reproductive strategies of plants are often
tive costs between plants that behave as males or as females
connected to the morphology of axes and to their position
may lead to dimorphism in secondary sexual characteristics
within the plant architecture. The coexistence of axes with
such as leaf area, internode size, the form of the canopy
different morphological characteristics, hereafter referred to
(Bond and Midgley, 1988; Kohorn, 1994), and in primary and
as axis polymorphism, is frequent and plays a role in plant
secondary growth characteristics (Verdú et al., 2007). Another
life strategies (Hallé et al., 1978; Suzuki, 2000; Hasegawa
example is the case of species living in a seasonal climate.
and Takeda, 2001; Remphrey et al., 2002; Kawamura and
Axis dimorphism (i.e. two morphologically distinct kinds of
Takeda, 2006). Axis polymorphism results from contrasting
axes) appear in the Mediterranean Cistus incanus subsp.
meristem expression and activity (Hallé et al., 1978). It is
incanus as the result of the seasonal adaptation of axis mor-
mainly related to axis orientation (vertical or orthotropy vs.
phology to the prevailing climatic conditions during the
horizontal or plagiotropy) or axis length (short axis vs. long
plant’s growth: short axes with few, densely packed, small
axis) (Bell, 1991; Barthélémy and Caraglio, 2007).
leaves when grown in summer, and long axes with many,
In most species, axis polymorphism is a main determinant of
large leaves when grown in winter and spring (Aronne and De
plant architectural organization. In particular, differentiation of
Micco, 2001).
axis size may affect several variables related to the stem (length,
Axis polymorphism does not concern only axis morphology
diameter, dry mass), to the leaves (area, dry mass) or both. As an
but axis functioning as well, and especially reproductive traits.
element of plant life strategy, axis polymorphism can express
Long and short axes are specialized in environmental explora-
tion and exploitation, respectively (Bell, 1991). A main differ-
* For correspondence. E-mail normand@cirad.fr
†
Present address: Département de Mathématiques, Université de Versailles
ence concerns flowering and fruiting: short axes generally bear
Saint-Quentin en Yvelines, 45 avenue des Etats-Unis, 78035 Versailles Cedex, flowers and fruit, and long axes are mainly vegetative (Bell,
France 1991). This phenomenon has been described and studied in
# The Author 2009. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved.
For Permissions, please email: journals.permissions@oxfordjournals.org
1326 Normand et al. — Architectural position, axis morphology and functional behaviour

some temperate fruit tree species such as apple (Malus (Suryanarayana, 1978; Pandey, 1988; Chacko, 1991;
domestica: Johnson and Lakso, 1986; Wünsche et al., 1996; Davenport and Nuñez-Elisea, 1997); a larger leaf area and
Wünsche and Lakso, 2000; Lauri and Kelner, 2001) and stem implies larger carbohydrate synthesis and storage,
cherry (Prunus avium: Lauri, 1992), as well as in temperate respectively. The hypothesis rested on two implicit assump-
forest tree species (Hasegawa and Takeda, 2001; Remphrey tions. First, no trade-off occurs among functions (vegetative
et al., 2002; Kawamura and Takeda, 2006). The location of growth and reproduction) at the GU level. Second, apical
the different kinds of axes within the canopy layers has been and lateral GUs are not functionally differentiated; they
characterized for some species (Hasegawa and Takeda, 2001; branch, flower and fruit in an equivalent manner, depending
Remphrey et al., 2002; Kawamura and Takeda, 2006); only on resource allocation to individual GUs. These assump-
however, only a few studies have dealt with their topological tions diverged from the knowledge available on the functional
location within the tree architecture (Suzuki, 2000). differentiation of axes (e.g. Bell, 1991; Hasegawa and Takeda,
Rather than the axis length itself, the predominance of stem 2001; Kawamura and Takeda, 2006), but formed a null
components over the foliar components, referred to as axializa- hypothesis in the case of mango, for which no data was avail-

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tion, determines the vegetative status of the axes in apple, able on the morphology and functional differentiation of GUs.
cherry and some tropical species (Lauri and Térouanne, We addressed the following questions. (1) Do apical and
1991; Lauri, 1992; Lauri and Kelner, 2001). The higher the lateral GUs of mango have different morphological traits?
axialization is, the more vegetative the axis will be. In contrast, (2) Are these differences cultivar-dependent? (3) Are these
the lower the axialization is, the more floriferous the axis will differences related to contrasted flowering, fruiting and branch-
be. This characteristic evolves during the plant’s life. As ing behaviours of apical and lateral GUs?
shown in the case of invasive bramble (Rubus alceifolius),
axialization is low during the first stages of growth, leading
to the rapid autotrophy of the plant, whereas it is high at the M AT E R I A L S A N D M E T H O D S
adult stage when the plant explores the environment (Baret
Field site and plant material
et al., 2003). In cherry, the axialization progressively decreases
as the tree ages, in parallel with the reduction of axis length The experimental orchard in which the study was conducted
and the development of flowering on the axes (Lauri, 1992). was located in a research station of the French Agricultural
Nonetheless, the effects of morphological dimorphism on Research Centre for International Development (CIRAD) in
functional traits other than flowering and fruiting have been Saint-Pierre, Reunion Island (208520 S, 558310 E) at
poorly investigated. In particular, branching is a point of inter- 280 m a.s.l. An automatic weather station located close to
est. If branching processes differ between dimorphic axes, the the orchard recorded climatic data. Trees of eight mango
tree architecture and form may be affected by the number and (Mangifera indica) cultivars grafted onto the same polyem-
the position of each kind of axis. bryonic rootstock, ‘Maison Rouge’, were planted in May
The identification, characterization and location of morpho- 2001, about 8 months after grafting. The homogeneity of the
logically and functionally different axes are of major import- nucellar rootstock seedlings was visually assessed at the
ance in fruit tree species. This knowledge provides insights nursery stage. The orchard was flat and the soil homogenous,
for a better understanding of the determinants of flowering but for ease of care among cultivars, planting was designed
and fruiting, and leads to practical recommendations for tree as plots of seven aligned trees per cultivar, repeated in
management in order to optimize fruit production and/or two blocks, yielding 14 trees per cultivar. Tree spacing was
quality (Wünsche et al., 1996; Wünsche and Lakso, 2000; 6  4 m, wide enough to avoid interactions between canopies
Lauri and Laurens, 2005; Stephan et al., 2007). Although during the study. Trees of a cultivar were therefore genetically
this knowledge has been developed over more than a century similar, and environmental differences between them were
for temperate fruit trees, data are lacking for tropical fruit minimal. Trees were drip-irrigated. Cultural practices were
species. Goguey (1997) contributed to this topic with an archi- those recommended by local extension services. Trees were
tectural analysis of mango seedling trees. He identified the not pruned after planting to enable the natural development
respective roles of the architectural units belonging to the of the canopy. The first crop was harvested at the beginning
Scarrone model, with orthotropic axes, rhythmic branching of 2004, two and a half years after planting.
and terminal flowering (Hallé et al., 1978), and reiteration Four of these cultivars, ‘Cogshall’, ‘Irwin’, ‘José’ and
characterized by a delayed growth of buds within the existing ‘Kensington Pride’, were chosen for the study on the basis
tree architecture. of their diverse origin, tree size, growth and flowering habits.
The present study focuses on the growth unit (GU), an ‘José’ is an Indian-type mango selected in the middle of the
elementary component of the axes forming the architectural 19th century in Reunion Island and is the main cultivar
unit. We have characterized two architecturally contrasted grown locally (Vincenot, 2004); it is a medium-sized tree
GUs (Hallé et al., 1978), the apical and the lateral GUs of with an open canopy. ‘Cogshall’ was selected in Florida
four mango (Mangifera indica) cultivars, both morphologi- (Campbell, 1992) and is grown locally for export; it is a
cally (stem length, leaf mass and area) and functionally medium-sized tree with a dense, compact canopy. ‘Irwin’
(branching, flowering and fruiting). We hypothesized that was selected in Florida; it is a small-to-medium-sized tree
apical GUs will have larger stem and leaf area and, conse- with an open canopy (Campbell, 1992; Knight, 1997).
quently, will be more likely to flower, fruit and branch. This ‘Kensington Pride’ is a commercial cultivar selected and
hypothesis was based on the suggested positive role of carbo- grown in Australia; it is a large, vigorous tree with a dense
hydrate availability for flowering and fruiting in mango spreading canopy (Knight, 1997). ‘Cogshall’ and ‘Irwin’
 Normand et al. — Architectural position, axis morphology and functional behaviour 1327

Study 1

Study 2

Study 3

Vegetative
Phenology

growth
Flowering
Fruit
growth

300
Rainfall (mm)

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250
200
150
100
50
0
Temperature (ºC)

30
27
24
21
18
15
6 8 10 12 2 4 6 8 10 12 2 4 6 8 10 12 2 4 6 8 10 12
Months
2003 2004 2005 2006

F I G . 1. Time scale of the studies performed, mango phenology, monthly rainfall and mean monthly temperatures at the experimental orchard (208520 S, 558310 E)
from June 2003 to December 2006.

tend to be regular bearers, whereas ‘Kensington Pride’ and the corresponding initial growth level G– 1 is the preceding
especially ‘José’ exhibit alternate bearing. growth level at which GUs grew and branched to produce
At the study site, mango trees flower from August to the growth level G. The initial growth level 0 thus corresponds
October and the harvest extends from the end of December to the terminal GUs of the previous growing season that
to March (Fig. 1). Vegetative growth begins slowly with flow- resulted in the first growth level of the current annual growth
ering, continues during fruit growth, and flushes after harvest (Fig. 2). Inflorescences appear apically on terminal GUs in
during the hot and rainy season, until May. About half of mango. Consequently, GUs that have already flowered can
the vegetative growth occurs after harvest. The vegetative only produce lateral GUs at the first growth level.
resting period separating two growing seasons, each of A mango inflorescence is composed of hundreds of
which includes the reproductive stages and vegetative individual flowers that open successively for a period of
growth, occurs from June to July, just before flowering of about 2 weeks. They are pollinated by insects, in particular
the next growing season. Morphological measurements were flies of several genera and bees. Because of the number of
performed during the vegetative resting period, after the last flowers per inflorescence, it is a time-consuming job to calcu-
GUs had matured and leaves were completely expanded. late a fruit-set rate as the ratio of the number of fruit to the
Mango trees have rhythmic and mainly sequential growth number of flowers per GU. Moreover, natural fruit drop
(Hallé et al., 1978). A resting period of a few weeks to a occurs during the month following fruit set. Consequently,
few months occurs between the end of the GU extension and and because the individual unit in this work was the GU, we
the burst of its apical and possibly lateral buds to give new considered that a GU flowered or fruited if it bore at least
GUs. During the growing season, a terminal GU produces one inflorescence or if it bore at least one fruit until harvest,
one-to-several GUs, among which can be distinguished an respectively.
apical GU stemming from the apical bud if present, and
none-to-several lateral GUs stemming from lateral buds.
These GUs can themselves grow and branch similarly during Effect of GU position on its morphology
the same growing season and produce successive growth The effect of GU position on its morphology was
levels constituting a current-year branch complex. Each gener- investigated in June 2004 and June 2006 on ten to 15 current-
ation of GUs during a growing season will hereafter be referred year branches randomly sampled each year on three to five
to as a growth level (Fig. 2). By definition, a growth level trees per cultivar. These branches were composed of one to
includes the GUs located at the same distance, expressed in 16 GUs arranged in successive (1 to 4) growth levels. The pos-
number of GUs, from the terminal GU of the previous ition (apical vs. lateral) of the basal GU of each branch was
growing season. For a given growth level G (G ¼ 1, 2, . . . ), recorded before sampling. Each GU of these branches was
1328 Normand et al. — Architectural position, axis morphology and functional behaviour

Growth
level 4 Current-year
branch complex

Growth

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level 3

Growth
level 2

Growth
level 1
Growth level 0

(growth unit of the previous

growing season)

F I G . 2. Schematic representation of a mango current-year branch complex composed of one apical branch and two lateral branches borne by a growth unit (GU)
of the previous year’s growing season (in black). Rectangles are GU stems; leaves are not represented. Apical GUs are in grey and lateral GUs are in white. The
dark grey circles are the potential apical sites for flowering. Growth levels are illustrated by arcs and numbered according to the order of development from the
beginning of the growing season.

identified as apical or lateral. They were then separated GUs of the 12 trees studied (three trees  four cultivars)
with pruning shears and individually subjected to the measure- were recorded as apical or lateral and labelled. The occurrence
ments detailed below. Overall, 306 GUs were sampled, 174 in of flowering was recorded on these GUs between July and
2004 and 132 in 2006. Sample size per cultivar is given in September 2003. The occurrence of fruiting was recorded
Table 1. from December 2003 to February 2004 during harvest.
Stem length was measured from the base to the apical bud Vegetative growth was recorded from August 2003 to May
of the GU stem. The leaves were counted, and individual 2004. Each new GU was identified as apical or lateral and
leaf area was measured with a planimeter (AM200, ADC labelled. The same observations were carried out during the
BioScientific Ltd., Hoddesdon, UK). The leaf area of a GU following growing season, from July 2004 to May 2005.
was the sum of the individual areas of its leaves. The leaves Overall, 11 756 GUs were recorded for this study.
of each GU were then oven-dried at 80 8C for 72 h and
weighed. Because of secondary growth in diameter on GUs
of branches composed of several growth levels, stem diameter Effect of GU position and diameter on flowering and fruiting
and dry weight were not relevant variables. Thus, it was not In the studies detailed above, morphology and functioning
possible to calculate the axialization index as the ratio of (branching, flowering and fruiting) of apical and lateral GUs
stem dry weight to leaf dry weight at the end of primary were measured and analysed separately on different trees in
growth (Lauri and Kelner, 2001) for each GU. To overcome the same orchard. Therefore, the interpretation of the
this problem, we approximated the axialization index as the relationships between morphology and functioning was
ratio of stem length to leaf dry weight, expressed in based on the average behaviour of apical and lateral GUs
mm g21. This value is the inverse of the linear density of for each cultivar. To further analyse the relationship
leaf dry weight along the stem and is an indicator of the between morphology and functioning and, in particular, to
balance between the stem and leaf components of the GU, determine whether or not the different flowering and fruiting
independent of the stem secondary growth. behaviours of apical and lateral GUs were related to their
respective size according to our hypothesis, we carried out
an additional study in the orchard, on the cultivar
Effect of GU position on branching, flowering and fruiting
‘Cogshall’ only. The objective was to establish the relation-
The effect of GU position on branching, flowering and ship between the diameter of the GU stem and flowering
fruiting was investigated non-destructively using a dataset and fruiting for apical and lateral GUs. GU diameter is allo-
resulting from an exhaustive topological description of GUs, metrically related to leaf mass and area of the GU (Normand
flowering and fruiting of three trees per cultivar during two et al., 2008) and is therefore an easy and non-destructive
growing seasons. During the 2003 rest period, all terminal estimator of GU morphology.
 Normand et al. — Architectural position, axis morphology and functional behaviour 1329

TA B L E 1. F- and P-values of the analyses of variance of the effects of growth unit (GU) position (apical, lateral), cultivar (4) and
year (2) and their interactions for six morphological variables describing the growth units of four mango cultivars: growth unit
length, number of leaves, leaf dry weight, individual leaf area, growth unit leaf area and axialization index

Individual leaf Axialization

Stem length No. of leaves Leaf d. wt area GU leaf area index

Effects d.f. F P F P F P F P F P F P

Position 1 24.0 ,0.001 490.9 ,0.001 391.1 ,0.001 195.4 ,0.001 449.2 ,0.001 245.6 ,0.001
Cultivar 3 65.1 ,0.001 40.4 ,0.001 27.9 ,0.001 26.1 ,0.001 47.2 ,0.001 16.4 ,0.001
Year 1 18.4 ,0.001 10.9 0.001 8.4 0.004 7.2 0.008 15.8 ,0.001 2.3 0.130
Position  cultivar 3 4.6 0.003 15.4 ,0.001 16.7 ,0.001 4.2 0.006 22.8 ,0.001 4.8 0.003
Position  year 1 0.9 0.346 16.3 ,0.001 14.4 ,0.001 6.5 0.011 22.5 ,0.001 3.5 0.061
Cultivar  year 3 4.3 0.005 6.8 ,0.001 1.6 0.192 2.6 0.049 3.7 0.012 1.2 0.293

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Position  cultivar  year 3 0.4 0.742 5.0 0.002 1.3 0.274 0.6 0.630 2.1 0.106 0.8 0.513
Residuals 290 – – – – – – – – – – – –

Sample size per cultivar: ‘Cogshall’, n ¼ 73; ‘Irwin’, n ¼ 64; ‘José’, n ¼ 64; ‘Kensington Pride’, n ¼ 105. d.f., degrees of freedom.

In June 2006, 1510 terminal GUs (606 apical and 904 were estimated and analysed for each growth level to
lateral) were randomly sampled and labelled on three trees account for possible contrasting branching behaviours
of the cultivar ‘Cogshall’. Their relative position was recorded between growth levels. Growth units produced later had less
and their basal diameter was measured with a digital calliper. time to grow again during the growing season, and we thus
The occurrence of flowering on these GUs was recorded from expected that Pvg would decrease as the growth levels
July to September 2006. Fruiting (occurrence and number of increased.
fruit per GU) was recorded in December 2006, after natural GLMs were estimated assuming that the occurrence of
fruit drop and before the beginning of harvest. vegetative growth (Pvg), flowering (Pflo), and fruiting (Pfru)
of a GU followed binomial distributions (Venables and
Ripley, 2002). Preliminary analysis of Dbr suggested an over-
Data analysis
dispersed Poisson distribution for this parameter, i.e. with
Statistical analyses were performed using R software variance larger than mean. GLMs were therefore estimated
(R Development Core Team, 2006). Morphological data for this parameter with a Poisson distribution and a dispersion
were subjected to a full model of analysis of variance (GU parameter larger than 1 to account for over-dispersion
position  cultivar  year). This was possible since the two (Venables and Ripley, 2002). GLMs were not estimated in
years could be considered independent because they were the case of very unbalanced samples or when sample size
not consecutive, and because of the random sampling of was lower than five GUs for at least one factor level.
branches each year on several trees. The year effect might Estimates of Pvg, Pflo, Pfru and Dbr for apical and lateral
reflect tree ageing and environmental influences. Although GUs and their 95 % confidence interval were calculated
the objective of the study was not to compare GU morphology from GLMs by Monte Carlo sampling (n ¼ 100 samples of
between cultivars, the cultivar factor was integrated into the two-thirds of the considered GU’s population), followed by
model to evaluate the contribution of each factor to explaining jackknifing (Efron, 1982).
the variability of GU morphology. Data from the third study, on cultivar ‘Cogshall’ only, were
The effect of GU position on branching, flowering and analysed according to Lauri and Trottier (2004). The GU basal
fruiting was analysed for each year and cultivar with general- diameter was measured with a digital calliper to the nearest
ized linear models (GLMs). The full model analysis was not 0.1 mm. Consequently, we had classes of GU diameter with
performed as previously described: in the second study, years a 0.1 mm span, which contained one-to-several GUs, each
were not independent since the GUs recorded in the second characterized by the occurrence of flowering and fruiting,
year were the descendants of the GUs recorded in the first and by the number of fruit (for those that bore fruit). For the
year. The cultivar effect could be related to genetic and to analyses, only classes with five or more GUs were considered
uncontrolled endogenous factors (e.g. phenology, previous in order to study flowering, and with five or more GUs that
yield) whose discussion was not the subject of this work. flowered in order to study fruiting. In order to have a large
Branching was described by two variables: the occurrence sample size, the classes with four or more GUs bearing fruit
of vegetative growth (Pvg), i.e. the occurrence of a terminal were considered to study the mean number of fruit per GU.
GU to produce at least one new GU, apical or lateral, For each class of diameter, the flowering rate was calculated
during a growing season; and branching density (Dbr), i.e. as the relative frequency of terminal GUs that flowered
the number of lateral GUs stemming from a GU where vege- (number of GUs that flowered/total number of GUs), the fruit-
tative growth occurred. Dbr was estimated separately for GUs ing rate was calculated as the relative frequency of terminal
bearing or not bearing an apical GU in order to account for GUs that flowered and bore at least one fruit until harvest
apical dominance. The total number of GUs stemming from (number of GUs that bore at least one fruit/number of GUs
a GU that branched was therefore Dbr þ 1 if an apical GU that flowered), and the mean number of fruit per GU was cal-
was present, and Dbr otherwise. Moreover, Pvg and Dbr culated for GUs that bore fruit. The relationships between
1330 Normand et al. — Architectural position, axis morphology and functional behaviour

flowering rate, fruiting rate and mean number of fruit per GU, on fruiting rate, GU diameter and mean number of fruit per
on the one hand, and GU diameter, on the other hand, were GU were tested with one-way analysis of variance.
compared for apical and lateral GUs.
A quadratic adjustment was made to the relationships
between the flowering rate and the GU diameter. A compari- R E S U LT S
son of maximum location (i.e. GU diameter at maximum flow-
ering rate) and maximum value (i.e., maximum flowering rate) Effect of GU position on its morphology
between curves of apical and lateral GUs was tested. To Except for stem length, the GU position was the main factor
compare maximum location between curves, a deviance explaining the variability of GU morphology, well ahead of
F-test between embedded models was set up, defining the the cultivar factor (Table 1). These two factors were highly
model with constraint of maximum located at the same place significant for all variables. Year was the less-explanatory
as the submodel. For comparison of maximum values, the single factor of the variability of GU morphology; its effect
standard error of the difference was calculated based on the was not significant for the axialization index. Results are pre-

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covariance matrix of the model parameters, and a Z-test was sented in Fig. 3 after pooling data from the two years.
then used. Linear adjustments were made to the relationships The effect of GU position indicated axis dimorphism in
between the fruiting rate and the GU diameter, and between these mango cultivars: apical GUs were longer, more leafy,
the mean number of fruit per GU and the GU diameter. To and had a lower axialization index than lateral GUs (Fig. 3).
compare slopes and intercepts for apical and lateral GUs, an Stem length was the variable the least affected by GU position.
F-test between three embedded models (different slopes and On average, apical GUs were 1.31 and 1.34 times longer than
intercepts, common slope and different intercepts, common lateral GUs for ‘Kensington Pride’ and ‘Cogshall’, respect-
slope and intercept) was set up. The effects of GU position ively. These differences were not significant for ‘Irwin’ and

350 30
A c c b a B bc c b a
300 *** 25 ***
Stem length (mm)

Number of leaves

Apical
250 Lateral ns 20
*** ***
200 * ***
ns 15
150
10
100
50 5

0 0
Mean individual leaf area (cm2)

30
C b b b a 70
D b c c a
25 ***
Leaf dry weight (g)

*** 60
20 50 *** ***
*** 40 ***
15
*** ***
30
10
20
5 10
0 0
1800 80
Axialization index (mm g–1)

E b bc c a F c bc a b
1500
GU leaf area (cm2)

*** ***
60
1200 ***
***
900 *** 40
*** *** ***
600
20
300

0 0
‘Cogshall’ ‘Irwin’ ‘Jose’ ‘K. Pride’ ‘Cogshall’ ‘Irwin’ ‘Jose’ ‘K. Pride’
Cultivar Cultivar

F I G . 3. Effect of growth unit (GU) position, apical or lateral as indicated, on (A) stem length, (B) number of leaves, (C) leaf dry weight, (D) mean individual leaf
area, (E) growth unit leaf area and (F) axialization index for four mango cultivars. Data for two years, 2004 and 2006, are pooled. Bars indicate s.e. For each
variable, cultivars with different letters have significantly different means (Tukey’s test, P , 0.05). The effect of growth unit position is indicated: ns, P . 0.05;
*, P , 0.05; ***, P , 0.001.
 Normand et al. — Architectural position, axis morphology and functional behaviour 1331

‘José’. The GU leaf area was 2.54– 3.47 times larger in apical morphological attributes of ‘Irwin’ GUs, and variables related
GUs than in lateral GUs. Leaf dry weight followed the same to leaves increased more for apical GUs than for lateral GUs
pattern because of similar values of specific leaf area (leaf between 2004 and 2006 (data not shown).
area per unit of leaf dry matter) among GU positions and cul-
tivars (data not shown). These pronounced differences in GU
leaf area between apical and lateral GUs were the consequence Effect of GU position on branching, flowering and fruiting
of not only a larger number of leaves per GU (1.49– 1.99 times As a general rule, apical GUs grew and branched more
larger among cultivars), but also of a larger individual leaf area (Table 2), and flowered and fruited more (Table 3) than
(1.46– 1.78 times larger among cultivars). Since the range of lateral GUs, indicating contrasting functioning between the
leaf area was larger than that of stem length, the axialization two GU types. For branching, results from 2005 are presented
index of apical GUs was 0.31– 0.41 times that of lateral GUs. in Table 2; similar results and trends were observed in 2004
Although the objective of this study was not to compare the (data not shown).
morphological attributes of the cultivars, it is interesting to The occurrence of vegetative growth, Pvg, decreased from

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note that the vigorous cultivar ‘Kensington Pride’ (Knight, the lower to the higher initial growth levels, justifying a pos-
1997) had the longest and most leafy GUs, with the largest teriori the analysis of this variable for each growth level
individual leaves (Fig. 3). The year effect expressed an (Table 2, statistical tests not shown). This pattern was
increase in GU morphological attributes between 2004 regular for ‘Irwin’ and ‘Kensington Pride’ for both years,
and 2006. but fluctuated somewhat for ‘Cogshall’ and ‘José’. In
The significant interactions between factors were related to general, apical GUs had a significantly higher Pvg than
different patterns of change of the variables with respect to lateral GUs, regardless of the growth level and the year.
these factors. They were more significant for variables related Some differences were not significant, but this hierarchy was
to leaves than for stem length and axialization index, in particu- respected in most of the cases. For a given cultivar and
lar for interactions involving GU position. This indicated that growth level, Pvg varied with year.
the effect of GU position differed among cultivars (Fig. 3) and The branching density, Dbr, also varied among growth levels
years. For example, the GU position has the lowest effect on and with the presence/absence of an apical GU, justifying

TA B L E 2. Occurrence of vegetative growth (Pvg) and branching density with presence (Dbr Aþ ) or absence (Dbr A2 ) of apical
dominance for apical and lateral growth units of different growth levels for four mango cultivars in 2005, assessed using generalized
linear models

‘Cogshall’ ‘Irwin’ ‘José’ ‘Kensington Pride’

Variable Initial growth level Apical Lateral Apical Lateral Apical Lateral Apical Lateral

Pvg 0 0.70a 0.47b 0.83a 0.45b 0.43 0.33 0.61a 0.35b

1 0.71a 0.09b 0.74a 0.32b 0.51 0.55 0.41a 0.05b
2 0.36a 0.20b 0.35 0.17 0.08a 0.01b 0.17a 0.07b
3 0.08a 0.02b (0.10) – – – – –
Dbr Aþ 0 2.60a 1.09b 0.15 0.22 2.67a 0.80b 2.37a 1.39b
1 0.85 0.69 0.15 0.00 1.20a 0.44b 2.27a 0.75b
2 1.77a 0.41b (0.00) – (0.21) – 1.70 0.37
3 (1.90) – – – – – – –
Dbr A 2 0 4.51a 2.46b 2.60a 1.37b 2.00 2.06 6.54a 3.97b

For each growth level and cultivar, different letters indicate significantly different values (P , 0.05); differences are not significant otherwise. Sample size
always .5. Values within parenthesis are estimated from the data but were not tested for the effect of growth unit position (very unbalanced samples). For
clarity, 95 % confidence intervals are not shown: their ranges vary between 0.002– 0.040 for Pvg; 0.022–0.160 for Dbr Aþ ; and 0.029– 0.158 for Dbr A2 .

TA B L E 3. Flowering (Pflo) and fruiting (Pfru) occurrence for apical and lateral growth units of four mango cultivars in 2004 and
2005, assessed using generalized linear models

‘Cogshall’ ‘Irwin’ ‘José’ ‘Kensington Pride’

Variable Year Apical Lateral Apical Lateral Apical Lateral Apical Lateral

Pflo 2004 0.79a 0.57b 0.79a 0.65b 0.40 0.35 0.89a 0.79b
2005 0.51 0.49 0.82a 0.70b 0.61a 0.45b 0.52 0.57
Pfru 2004 0.52a 0.24b 0.45a 0.27b 0.69a 0.39b 0.71a 0.44b
2005 0.31 0.25 0.43a 0.32b 0.39a 0.14b 0.51a 0.29b

For each cultivar and year, different letters indicate significantly different values between the two positions (P , 0.05); differences are not significant
otherwise. For clarity, 95 % confidence intervals are not shown; their ranges vary between 0.003– 0.016 for Pflo and 0.005 –0.020 for Pfru.
1332 Normand et al. — Architectural position, axis morphology and functional behaviour

a posteriori the analysis per level of these factors (Table 2, 1·0 A

statistical tests not shown). As a general rule, apical GUs
had a higher branching density than lateral GUs. Across all
0·8
cultivars, growth levels and years, they significantly produced
0.73– 1.87 more GUs than lateral GUs with apical dominance,

Flowering rate
and 0.67– 2.57 more GUs otherwise. Apex growth did not 0·6
strongly repress the simultaneous growth of lateral meristems,
indicating a rather mild apical dominance. However, cultivars 0·4
differed in their sensitivity to apical dominance, e.g. the rela-
tive increase of Dbr in the absence of apical dominance was
larger for ‘Irwin’ and ‘Kensington Pride’ than for ‘Cogshall’ 0·2
Apical
and ‘José’ (statistical tests not shown). Dbr without apical dom- Lateral
inance was calculated for the initial growth level 0 only, where 0·0

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apical flowering on some GUs prevented the development of
new apical GUs. 1·0
The occurrence of flowering, Pflo, was significantly higher B
for apical than for lateral GUs in five out of eight cultivar 
0·8
year combinations, and was not significant in three out of
eight combinations (Table 3).

Fruiting rate
The occurrence of fruiting, Pfru, was significantly higher for 0·6
apical than for lateral GUs in seven out of eight cultivar  year
combinations; it was not significantly higher for ‘Cogshall’ in
0·4
2005 (Table 3). These results suggested that the GU position
had a greater effect on fruiting than on flowering. This was
also supported by the higher mean ratio of apical value to 0·2
lateral value for Pfru than for Pflo for each cultivar  year com-
bination (mean + s.e.: 1.79 + 0.17 for Pfru vs. 1.17 + 0.06 for 0·0
Pflo; P , 0.01).
2·5 C
Effect of GU position and diameter on flowering and fruiting
Mean number of fruit per GU

The relationships between GU diameter and flowering rate 2·0

for apical and lateral GUs were quadratic but differed in
their patterns (Fig. 4A). The maximum flowering rates of 1·5
each curve were significantly different (0.89 and 0.75 for
apical and lateral GUs, respectively; P , 0.001), and the pos-
1·0
ition of the maximum also differed (6.8 mm and 4.5 mm for
apical and lateral GUs, respectively, P , 0.001). Beyond the
maximum value, the flowering rate decreased as the GU diam- 0·5
eter increased. This decrease was sharper and affected GUs
with a smaller diameter for lateral than for apical GUs. The 0·0
curve fitted for apical GUs was always above the curve fitted
2 3 4 5 6 7 8 9
for lateral GUs, indicating that for a given GU diameter,
Growth unit diameter (mm)
apical GUs were more likely to flower than lateral GUs over
the range of GU diameters in our dataset. This was especially F I G . 4. Relationships between (A) flowering rate, (B) fruiting rate and (C)
true for GU diameters greater than approx. 5 mm. mean number of fruit per growth unit (GU) and growth unit diameter for
apical and lateral terminal GUs as indicated for the mango cultivar
The fruiting rate was linearly related to the GU diameter, ‘Cogshall’ in 2006. Quadratic relationships for flowering rate were as
independently of the GU position (Fig. 4B). In the embedded follows: apical GUs, y ¼ 20.017x 2 þ 0.230x þ 0.103, n ¼ 47, R 2 ¼ 0.19,
linear models tested (different slopes and intercepts, common P ¼ 0.01; lateral GUs, y ¼ 20.076x 2 þ 0.691x 20.822, n ¼ 47, R 2 ¼ 0.49,
slope and different intercepts, common slope and intercept), P , 0.001. The linear relationship for fruiting rate was y ¼ 0.059x þ 0.041,
the GU diameter effect was always significant (P , 0.01), n ¼ 82, r 2 ¼ 0.24, P , 0.001. No relationship was observed between the
mean number of fruit per growth unit and growth unit diameter (n ¼ 49,
whereas the GU position effect and the interaction were not r 2 ¼ 0.001, P ¼ 0.81).
significant. The simpler model with a common slope and inter-
cept was therefore retained (F-test comparison with the differ-
ent slopes and intercepts model: P ¼ 0.86). The mean fruiting mean diameter of apical GUs (6.2 mm and 4.5 mm for
rate was significantly higher for apical than for lateral GUs apical and lateral GUs, respectively; P , 0.001).
(0.41 and 0.30, respectively; P , 0.01), in accordance with The mean number of fruit per fruiting GU was variable,
the results obtained in the second study (Table 3). Since the between 1.0 and 2.2, with a mean value (+ s.e.) of 1.48 +
two types of GUs shared the same relationship between GU 0.05 (Fig. 4C). It was, however, independent of the GU pos-
diameter and fruiting rate, this was related to the larger ition and diameter (P ¼ 0.99 for position effect, P ¼ 0.89
 Normand et al. — Architectural position, axis morphology and functional behaviour 1333

for diameter effect, P ¼ 0.89 for position  diameter inter- The occurrence of vegetative growth tended to decrease with
action in the linear model with different slopes and intercepts). increasing growth level. Pvg variability across years suggested
that factors other than GU position and growth level affected
this parameter. For the initial growth level 0 (i.e. GUs of the
D IS C US S IO N previous growing season), the occurrence of flowering and
fruiting on some GUs at the beginning of the growing
Morphological variability between apical and lateral growth units season might have affected their subsequent growth. For the
The results revealed GU dimorphism in the four mango culti- initial growth levels 1, 2 and 3, Pvg variability could have
vars studied in relation to the relative position, apical or lateral, been linked to the fact that Pvg was probably more closely
of the GU. Growth unit dimorphism was more conspicuous for related to the date of appearance of each GU than to the
leaf characteristics than for stem length. As a consequence, the growth level itself. Growth units that appeared early in the
axialization index was lower on apical GUs (Fig. 3), indicating growing season were more likely to grow during the same
a higher linear density of leaf dry weight on these GUs. The season than late GUs. The initial growth levels 2 and 3 were

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four cultivars exhibited the same pattern of differences mainly composed of GUs that appeared late in the growing
between apical and lateral GUs, but with a cultivar effect on season, and consequently had lower Pvg as growth level
GU morphology and on dimorphism intensity (interaction increased. In contrast, the initial growth level 1 was a
between GU position and cultivar; Table 1). mixture of GUs that appeared early and late (and which did
Because of GU secondary growth in diameter for branches not grow further) in the growing season. Pvg then depended
composed of several growth levels, stem diameter was not con- on the balance between early and late GUs. Although the
sidered as a pertinent morphological variable. On these four effect of GU position was demonstrated with our data,
cultivars, the total leaf area and dry weight of a branch are further studies are required to investigate the effect of other
allometrically related to the branch basal cross-sectional area factors on branching.
or to the basal diameter (Normand et al., 2008). This was At the GU level, apical dominance appeared mild and
true in particular for branches composed of a single GU, i.e. cultivar-dependent in mango. Differences in branching
before secondary growth. This suggests that apical GUs have density between apical and lateral GUs could be viewed as
a larger initial basal diameter (before secondary growth) an example of apical control at the branch level (Cline,
than lateral GUs, in relation to their larger leaf area. This 1997), where branching of an apical GU has a depressive
was supported for ‘Cogshall’ by the results of the third study effect on branching of the lateral GUs of the same growth
on terminal GUs (Fig. 4). Consequently, the stem of apical level (Fig. 2). As for flowering and fruiting, it would be inter-
GUs was longer, at least for ‘Cogshall’ and ‘Kensington esting to investigate the relationship between GU diameter,
Pride’, and thicker than the stem of lateral GUs, indicating a GU position and branching, in particular to clarify if there is
larger GU volume. a functional differentiation of apical and lateral GUs for this
The year effect could reflect ontogenetic development of the process.
tree and environmental influences. The weather – mean temp-
erature, rainfall (Fig. 1) and global solar radiation (data not Relationships between growth unit position, morphology,
shown) – was relatively similar during the 2004 and the and flowering and fruiting
2006 growing seasons. The larger GU morphological attributes
during the 2006 growing season than during the 2004 one Flowering and fruiting rates were both affected by GU
suggested that these young trees (3– 5-years old) were still in position, and they were higher for apical than for lateral
a phase of vegetative development of the canopy, and that GUs. In general, short axes bear flowers and fruit, and long
tree ageing had not yet occurred. axes are more vegetative (Bell, 1991); this phenomenon is
well known in apple (Wünsche et al., 1996; Lauri and
Kelner, 2001; Webster, 2005) and in cherry (Lauri, 1992;
Thompson, 1996). In contrast, if we consider mango apical
Effect of growth unit position on branching
GUs as long GUs, and lateral GUs as short GUs, our
Besides their morphological differences, the two types of results showed that the long GUs had the higher capacity
GUs behaved differently with respect to branching. The occur- to flower and especially to fruit. In that case, could apical
rence of vegetative growth, Pvg, and branching density, Dbr, (long) GUs and lateral (short) GUs of mango be related to
were both affected by GU position, independently of the exploration and exploitation structures, respectively (Bell,
growth level (Table 2). Apical GUs tended to branch more 1991)? The answer is probably no; first, because of their
than lateral GUs. Significant differences were more numerous reproductive behaviour and, second, because of the small
in 2005 than in 2004, suggesting a year effect, which was prob- differences in stem length between apical and lateral GUs
ably a combination of climate (there was more rainfall during of mango (Fig. 3) compared to the large differences gener-
the 2005 growing season than the 2004 one: 901 vs. 665 mm ally observed between long and short axes. This indicated
from August 1 to May 31, respectively; Fig. 1) and of fruit a lack of functional differentiation between apical and
load (heavier in the 2005 growing season for the four culti- lateral GUs with respect to exploration and exploitation.
vars). Differences between the two years were nevertheless From an evolutionary point of view, the longer stem of the
difficult to explain with our data alone. The differences were most floriferous apical GUs might be an adaptive advantage
more consistently significant for ‘Cogshall’ for the two since it can improve the floral display of mango apical
years, suggesting a cultivar effect. inflorescences.
1334 Normand et al. — Architectural position, axis morphology and functional behaviour

On the other hand, the lower axialization index of apical The linear relationship between fruiting rate and GU diam-
GUs in mango was linked to a higher occurrence of flowering eter, independent of the GU position, indicated that morpho-
(Fig. 3, Table 3), consistent with similar results in temperate logical differences between apical and lateral GUs
and tropical species (Lauri and Térouanne, 1991; Lauri, significantly contributed to explaining the differences in fruit-
1992; Lauri and Kelner, 2001). In mango, a negative relation- ing rate. This result was in accordance with the hypothesis that
ship between the axialization index and fruiting was observed. carbohydrates play a major role in mango fruiting (Davenport
It therefore seems that the predominance of the foliar com- and Nuñez-Elisea, 1997). However, differences in GU diam-
ponents over the stem components in mango is related to eter can also positively affect stem hydraulic characteristics
increased flowering and fruiting as well. (Tyree and Zimmermann, 2002), and consequently fruit set
The analysis of architectural development of mango seed- and retention. Further analyses would be necessary to clarify
lings allowed Goguey (1997) to identify five types of axes in the role of GU size on GU photosynthesis, carbohydrate
the mango canopy. Among them, the delayed proleptic axes, content and hydraulic characteristics in relation to fruiting.
which appear on trees older than 4 years old, are more florifer- In addition to this initial hypothesis, another one related to

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ous than the others. To link these results to our study is diffi- allometry could be proposed. Corner’s rule on axis conformity
cult because of methodological differences (climatic (Corner, 1949; Hallé et al., 1978) states that ‘the stouter, or
conditions, study unit) and differences in plant material (culti- more massive the axis in a given species, the larger and
var, young trees and sequential growth in our study); however, more complicated its appendages’ (leaves, inflorescences,
it would be interesting to study the within-canopy variability fruit). In particular, the relationship between stem diameter
of functional behaviour of apical and lateral GUs in relation and inflorescence size have been verified with different
to the architectural structures of old mango trees. Leucadendron species (Midgley and Bond, 1989). Normand
Our hypothesis, based on the suggested role of carbohydrate et al. (2008) showed that the relationship between stem size
availability for flowering and fruiting in mango (Suryanarayana, and leaf size remained valid at the cultivar level in mango.
1978; Pandey, 1988; Chacko, 1991; Davenport and Assuming that Corner’s rule in relation to reproductive
Nuñez-Elisea, 1997), predicted a positive relationship between organs remains valid at the cultivar level, then GUs with
GU diameter, an estimator of leaf area and stem size (Normand larger diameters would have a larger inflorescence (our unpub-
et al., 2008), and flowering and fruiting: larger leaf area indicates lished experimental results support this hypothesis), i.e. an
a larger photosynthetic surface, and larger stems represent a larger inflorescence with more flowers and a longer display for polli-
local storage capacity for carbohydrates and a higher capacity for nators. Consequently, their fruiting rate would be improved,
assimilate transport. The results for the average morphology and which was consistent with our results. The variability around
the average behaviour of apical and lateral GUs (first and second the fitted line (Fig. 4B) suggested, however, that factors
studies) supported this hypothesis. Results of the third study, at the other than GU diameter affected fruiting.
GU level for the cultivar ‘Cogshall’, supported this prediction for In contrast to previous research that has focused mainly on
fruiting but not for flowering (Fig. 4). The quadratic relationship the relationship between shoot morphology and flowering
between GU diameter and flowering showed that there was an (Remphrey et al., 2002; Kawamura and Takeda, 2006), we
optimal diameter corresponding to the maximal flowering rate. simultaneously investigated the relationships between shoot
Consistent with results from the second study, the optimal diam- morphology and flowering and fruiting. The contrasting
eter and maximum flowering rate were different for apical and relationships between GU diameter on the one hand, and flow-
lateral GUs. The flowering rate of lateral GUs was more sensitive ering and fruiting on the other, showed that if vegetative fea-
to GU diameter, as indicated by the sharper curvature of the tures were clearly involved in the determinism of flowering
relationship. and fruiting, the underlying rules were not the same.
Similar non-linear relationships between shoot morphology Fruiting was linearly size-related to the GU, whereas flowering
and flowering have been observed for several temperate forest was not, which could explain the greater impact of GU diam-
tree species: Alnus hirsuta var. sibirica (Hasegawa and Takeda, eter on fruiting than on flowering observed in the second study.
2001), Fraxinus pennsylvanica var. subintegerrima (Remphrey With reference to the assumptions supporting our general
et al., 2002), Vaccinium hirtum (Kawamura and Takeda, 2006) hypothesis, this suggested that apical and lateral GUs were
and apple (Lauri and Trottier, 2004). Shoot morphology was rep- functionally differentiated for flowering, but not for fruiting.
resented by shoot length in the first three species, and by the The mango tree has high direct costs of reproduction
number of leaves of the shoot in the latter species. Kawamura because of large and heavy fruit (Hasegawa and Takeda,
and Takeda (2006) proposed a hypothesis for this non-linear 2001). The linear, non-limiting, positive relationship between
pattern based on size-related changes in shoot-level resource GU diameter and fruiting could be detrimental to tree develop-
availability and costs of flowering on subsequent vegetative ment and survival because of excessive carbohydrate reserve
growth. The lower degree of flowering on small and, to a lesser exhaustion, for example if growing conditions favoured large
extent, on large shoots could then be explained in different GUs. In this context, the quadratic relationship between GU
ways (Hasegawa and Takeda, 2001; Kawamura and Takeda, diameter and flowering appeared as a means for the tree to
2006). Within the framework of this hypothesis, small shoots limit, at an earlier phenological stage, direct reproduction
would have a shortage of resources for reproduction and large costs by limiting the occurrence of flowering on large GUs.
shoots would have too high a flowering cost in terms of the max- Factors associated with GU architectural position were
imization of their life-time reproductive success. Further studies clearly involved in mango flowering. Two related questions
on the costs of reproduction in mango are needed to determine could therefore be raised. What are these factors? And why
if this hypothesis is supported by our results. do the thickest GUs have a lower flowering rate? Specific
 Normand et al. — Architectural position, axis morphology and functional behaviour 1335

studies, for example on the costs of reproduction (Kawamura Cabeu for their helpful contributions to field and laboratory
and Takeda, 2006), are necessary to investigate these ques- work, as well as two anonymous referees for their valuable
tions. However, one factor could be eliminated from the poten- comments on a previous version of the manuscript.
tial candidates: the florigenic promoter. It has been
hypothesized that the vegetative or reproductive fate of buds
in mango involves the interaction of a florigenic promoter L I T E R AT U R E CI T E D
and a vegetative promoter (Reece et al., 1949; Kulkarni,
1986, 1988; Davenport and Nuñez-Elisea, 1997; Davenport Aronne G, De Micco V. 2001. Seasonal dimorphism in the Mediterranean
Cistus incanus L. subsp. incanus. Annals of Botany 87: 789–794.
et al., 2006; Wilkie et al., 2008). The florigenic promoter is Baret S, Nicolini E, Le Bourgeois T, Strasberg D. 2003. Developmental pat-
synthesized in leaves in the presence of light and cool tempera- terns of the invasive bramble (Rubus alceifolius Poiret, Rosaceae) in
tures, and moves through the phloem to buds where it contrib- Reunion Island: an architectural and morphometric analysis. Annals of
utes to floral induction. A larger leaf area in apical GUs might Botany 91: 1 –10.
Barthélémy D, Caraglio Y. 2007. Plant architecture: a dynamic, multilevel
suggest that a larger amount of florigenic promoter is syn- and comprehensive approach to plant form, structure and ontogeny.

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thesized, consequently leading to a higher flowering rate. Annals of Botany 99: 375– 407.
Our results did not support this hypothesis because of the Bell A. 1991. Plant form. An illustrated guide to flowering plant morphology.
decrease in the flowering rate for larger GU diameters, i.e. Oxford: Oxford University Press.
larger GU leaf area. This hypothesis is no longer supported Bond WJ, Midgley JJ. 1988. Allometry and sexual differences in leaf size.
The American Naturalist 131: 901– 910.
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on a terminal GU, and that the florigenic promoter can be Chacko EK. 1991. Mango flowering – still an enigma. Acta Horticulturae
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Cline MG. 1997. Concepts and terminology of apical dominance. American
ing (Davenport et al., 2006). Consequently, the amount of Journal of Botany 84: 1064–1069.
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GUs was largely sufficient to ensure maximal flowering on of Botany 13: 367– 414.
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locatable florigenic promoter in mango. Scientia Horticulturae 110:
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