Reproductive phenology of two Mimusops species in relation to climate, tree diameter and canopy position in Benin (West Africa)

Abstract

Assessing species phenology provides useful understanding about their autecology, to contribute to management strategies. We monitored reproductive phenology of Mimusops andongensis and Mimusops kummel, and its relationship with climate, tree diameter and canopy position. We sampled trees in six diameter classes and noted their canopy position. For both species flowering began in the dry season through to the rainy season, but peaked in the dry season, whilst fruiting occurred in the rainy season and peaked during the most humid period. Flowering was positively correlated with temperature. Conversely, fruiting was negatively correlated with temperature and positively with rainfall, only in the Guineo-Sudanian zone. For M. andongensis, flowering and fruiting prevalences were positively linked to stem diameter, while only flowering was significantly related to canopy position. For M. kummel, the relationship with stem diameter was significant for flowering prevalence only and in the Guineo-Sudanian zone. Results suggest that phylogenetic membership is an important factor restricting Mimusops species phenology. Flowering and fruiting of both species are influenced by climate, and consequently climate change might shift their phenological patterns. Long-term investigations, considering flowering and fruiting abortion, will help to better understand the species phenology and perhaps predict demographic dynamics.

Full text

ORIGINAL ARTICLE
Reproductive phenology of two Mimusops species in
relation to climate, tree diameter and canopy position in
Benin (West Africa)
Gis
ele K. Sinasson Sanni
1,2
|
Charlie M. Shackleton
3
|
Brice Sinsin
1
1
Laboratoire d’Ecologie Appliqu
ee, Facult
e
des Sciences Agronomiques, Universit
e
d’Abomey-Calavi, Cotonou, B
enin
2
Laboratoire de Biomath
ematiques et
d’Estimations Foresti
eres, Facult
e des
Sciences Agronomiques, Universit
e
d’Abomey-Calavi, Cotonou, B
enin
3
Department of Environmental Sciences,
Rhodes University, Grahamstown, South
Africa
Correspondence
Gis
ele K. Sinasson Sanni
Email sinasson.gisele@gmail.com
Funding information
International Foundation for Science (IFS),
Grant/Award Number: D/5467-1; OWSD
(Organization for Women in Science for the
Developing World); SIDA (Swedish
International Development Cooperation
Agency)
Abstract
Assessing species phenology provides useful understanding about their autecology,
to contribute to management strategies. We monitored reproductive phenology of
Mimusops andongensis and Mimusops kummel, and its relationship with climate, tree
diameter and canopy position. We sampled trees in six diameter classes and noted
their canopy position. For both species flowering began in the dry season through
to the rainy season, but peaked in the dry season, whilst fruiting occurred in the
rainy season and peaked during the most humid period. Flowering was positively
correlated with temperature. Conversely, fruiting was negatively correlated with
temperature and positively with rainfall, only in the Guineo-Sudanian zone. For
M.andongensis, flowering and fruiting prevalences were positively linked to stem
diameter, while only flowering was significantly related to canopy position. For
M.kummel, the relationship with stem diameter was significant for flowering preva-
lence only and in the Guineo-Sudanian zone. Results suggest that phylogenetic
membership is an important factor restricting Mimusops species phenology. Flower-
ing and fruiting of both species are influenced by climate, and consequently climate
change might shift their phenological patterns. Long-term investigations, considering
flowering and fruiting abortion, will help to better understand the species phenology
and perhaps predict demographic dynamics.
R
esum
e
L’
evaluation de la ph
enologie d’une esp
ece fournit un 
eclairage int
eressant sur son
aut
ecologie, qui peut contribuer aux strat
egies de gestion. Nous avons suivi la
ph
enologie reproductrice de Mimusops andongensis et de Mimusops kummel et leur
relation avec le climat, le diam
etre des arbres et la position de la canop
ee. Nous
avons class
e nos 
echantillons d’arbres dans six classes de diam
etre et not
e la posi-
tion de leur canop
ee. Chez les deux esp
eces, la floraison a commenc
e pendant la
saison s
eche et s’est poursuivie durant toute la saison des pluies, avec un pic en sai-
son s
eche, alors que la fructification avait lieu en saison des pluies avec un pic dur-
ant la p
eriode la plus humide. La floraison 
etait positivement li
ee 
a la temp
erature.
Inversement, la fructification 
etait n
egativement li
ee 
a la temp
erature et positive-
ment li
ee aux chutes de pluie, mais uniquement en zone guin
eo-soudanienne. Pour
M. andongensis, la pr
evalence de la floraison et de la fructification 
etait li
ee positive-
ment au diam
etre des troncs, alors que seule la floraison 
etait significativement li
ee
Accepted: 17 July 2017
DOI: 10.1111/aje.12457
Afr J Ecol. 2017;1–11. wileyonlinelibrary.com/journal/aje ©2017 John Wiley & Sons Ltd
|
1


a la position de la canop
ee. Pour M. kummel, la relation avec le diam
etre des troncs

etait seulement significative pour la position de la canop
ee et dans la zone guin
eo-
soudanienne. Nos r
esultats sugg
erent que l’appartenance phylog
en
etique est un fac-
teur important qui limite la ph
enologie des esp
eces de Mimusops. La floraison et la
fructification des deux esp
eces sont influenc
ees par le climat et, par cons
equent, les
changements climatiques peuvent modifier leur sch
ema ph
enologique. Des 
etudes
plus longues, portant sur la floraison et les 
echecs de fructification, permettront de
mieux comprendre la ph
enologie des esp
eces et, peut-^
etre, de pr
edire la dynamique
de leur d
emographie.
KEYWORDS
climatic conditions, flowering, fruiting, Mimusops andongensis,Mimusops kummel, tree size
1
|
INTRODUCTION
Understanding the autoecology of species has been widely recognized
as an essential contribution to effective conservation strategies (Her-
rero-Jauregui, Sist, & Casado, 2012). An important aspect of species
autecology is the assessment of patterns of both their vegetative and
reproductive phenology (Wolkovich, Cook, & Davies, 2014). Research
on phenological processes can help in understanding the distribution,
ecology and dynamics at both species and community levels (Menga,
Bayol, Nasi, & Fayolle, 2012; Morellato et al., 2016). However, this
understanding could be limited by the potential confounding influence
of pollinator availability and seed dispersal, and responses of individual
trees to environmental stresses (Chuine, 2010; Morin, Viner, & Chuine,
2008). For Schwartz (2013), plant phenology is an integrative measure
of plant species responses to shifts in climatic and other environmental
factors, at local and global levels. Phenological processes can also
serve as an indicator of the health of species and ecosystems (Morel-
lato et al., 2016), and serve in regulating the fitness of individuals
(Munguia-Rosas, Ollerton, Parra-Tabla, & De-Nova, 2011). Indeed, the
ability of plant species to realize their vegetative and reproductive
phases determines population survival (Chuine, 2010; Okullo, Hall, &
Obua, 2004). Plant phenology is the study of bud and leaf develop-
ment, flowering, fruit production and leaf fall in relation to different
biotic and abiotic signals (Schwartz, 2013). Therefore, phenological
studies provide information on plant species functional rhythms but
also how they reflect biotic and abiotic environmental characteristics.
Local and viable management and conservation strategies based on
reproductive processes are thus useful, especially when habitat and
species integrity is under threat (Morellato et al., 2016).
Various abiotic and biotic factors may affect plant phenology
(Wolkovich et al., 2014). Abiotic drivers include climate (e.g. temper-
ature, humidity, rainfall and irradiance), soil (e.g. moisture, nutrients)
and topography (Lobo et al., 2003; Shackleton, 1999). However,
most studies indicate climate, through the three components of rain-
fall, temperature and photoperiod, as an essential factor influencing
plant phenology in tropical areas (Morellato, Camargo, & Gressler,
2013; Wolkovich et al., 2014). Indeed, these three components
control access to soil nutrients. In contrast, in semi-arid and arid
zones, soil moisture is a key determinant of phenological pattern
(Crimmins, Crimmins, & Bertelsen, 2011). As phenology is mainly
affected by climate, it has consequences on other ecosystem pro-
cesses due to other organisms’dependency on plants (Morellato
et al., 2016). Thus, the study of phenophases and factors that influ-
ence them is important to understand population and ecosystem
dynamics. This is also necessary for assessing potential climate
change impacts on species populations (Rosemartin et al., 2014).
Besides abiotic cues, plant size is an important biotic factor that
influences flowering and fruiting patterns of trees by shaping the acqui-
sition of resources (Fernandez Otarola, Sazima, & Solferini, 2013).
Knowing the stem diameter of reproductive maturity is relevant for set-
ting the diameter of exploitation of tree species (Plumptre, 1995). Fur-
thermore, tree position in the canopy is an important characteristic
which can affect reproductive ability of individual plants (Menga et al.,
2012). Indeed, canopy position defines the photoperiod at the individual
level, depending on the openness of the vegetation. Additional biotic
influences on phenological patterns include competition for pollinators
and other resources (Lobo et al., 2003). Also, plant phenology may be
strongly constrained by phylogenetic history and members of the same
genus or family may have similar phenological patterns. However, in
some cases, two species of the same genus may display different phe-
nological patterns, rather related to climatic factors (McIntosh, 2002).
Although the success of reproductive phenology of plant species is
highly determined by diverse biotic and abiotic factors, knowledge of
factors that influence reproductive phenology is still limited for most
species, especially in tropical areas (Fernandez Otarola et al., 2013;
Lobo et al., 2003). Understanding phenological patterns can help in
assessing the vulnerability of species populations (Chuine & Beaubien,
2001). Yet, many African countries lack studies on phenology and repro-
ductive biology of multiple important species (Menga et al., 2012), espe-
cially indigenous fruit species (Chikamai, Eyog-Matig, & Mbogga, 2006).
In this study, we compared the phenological patterns of Mimu-
sops andongensis Hiern and Mimusops kummel Bruce ex A. DC in
Benin and investigated how climate, plant size and canopy position
influence these. Mimusops species are important multipurpose trees
2
|
SINASSON SANNI ET AL.

mainly exploited for their fruits, bark and leaves (Sinasson S, Shackle-
ton, Assogbadjo, & Sinsin, 2017). For instance, in Cote d’Ivoire, the
bark of M.andongensis is exploited as medicine to treat skin and
stomach infections (Soro, Kone, & Kamanzi, 2010). In Benin, the bark
and leaves are used to treat different diseases, and the fruits are
consumed, especially by children and hunters, though not commer-
cialized (Sinasson S, Shackleton, Assogbadjo, et al., 2017). In Ethio-
pia, the fruits of M.kummel are commercialized raw or prepared
(Wondimu, Asfaw, & Kelbessa, 2006) and according to Teketay, Sen-
beta, Maclachlan, Bekele, and Barklund (2010), the species has pro-
spects for agro-industrialization as jams and jellies. This could also
be the case for M.andongensis. In Benin, the two species have simi-
lar uses although they occur in different areas and are exploited by
different ethnic groups (Sinasson S, Shackleton, Assogbadjo, et al.,
2017). Fruits of both species are consumed by birds and other ani-
mals such as monkeys (e.g. Kagoro-Rugunda & Hashimoto, 2015;
Moscovice et al., 2007; Nombim
e & Sinsin, 2003). Furthermore, a
study on the pollen characterization of honey produced in the Mani-
gri District in the northern part of Benin has identified M.kummel as
the most important source of pollen (Tossou et al., 2011), although
it is the second least abundant species in the area (Yedomonhan,
Adomou, Akoegninou, & de Foucault, 2012).
The objectives of this work were to (i) compare the reproductive
phenology patterns of M.andongensis and M.kummel in Benin, (ii)
identify how climatic characteristics influence the reproductive phe-
nology of the two species and (iii) assess the influence of tree diam-
eter and canopy position on phenological patterns. We hypothesized
that (i) reproductive phenology patterns differ between the two spe-
cies and (ii) the phenological patterns are strongly correlated with cli-
mate (rainfall and temperature), tree diameter and canopy position.
Mimusops andongensis and M.kummel trees bear leaves all year
round, and thus, this study did not include leaf phenology.
2
|
METHODS
2.1
|
Study area
The study was conducted in the three climatic zones of Benin, West
Africa (6°100
–12°250N and 0°450
–3°550E; Figure 1). In the Guineo-
Congolian zone, the climate is characterized by two rainy seasons (one
from mid-March to mid-July and one from mid-September to mid-
November) alternating with two dry seasons (one from mid-November
to mid-March and one from mid-July to mid-September). Annual rain-
fall varies between 900 mm and 1,300 mm; the mean annual tempera-
ture varies from 25 to 29°C and the relative humidity between 69%
and 97%. The Guineo-Sudanian zone is characterized by a transition
towards a unimodal rainfall regime with one rainy season (April to
November) and one dry season (December to April). Annual rainfall
varies between 1,100 mm and 1,200 mm; the annual temperature
ranges from 25 to 40°C and the relative humidity varies between 31%
and 98%. In the Sudanian zone, the climate is dry tropical with one
rainy season (April to October) and one dry season (November to
March). Annual rainfall varies between 950 mm and 1,150 mm; the
average temperature varies from 24 to 31°C and the relative humidity
between 18% and 99% (Adomou, 2010). Figure 2 presents monthly
rainfall and temperatures for the study period relative to the long-term
means. The Guineo-Congolian zone is dominated by relics of semi-
deciduous forests and Guinean savannahs. The Guineo-Sudanian zone
is characterized by a mosaic of woodlands, dry dense forests, tree and
shrub savannahs and riparian forests, and the Sudanian zone by savan-
nahs and riparian forests dominated by small diameter trees (Adomou,
Sinsin, & van der Maesen, 2006).
2.2
|
Data collection
We sampled 234 plots in seven forests (Lama, Assant
e, Agoua,
Monts-Kouff
e, Wari-Maro, Ou
em
e-Sup
erieur and Tanougou) dis-
tributed among the three climatic zones, based on the size of the
site and the abundance of Mimusops trees (Figure 1), with only Lama
Forest reserve for M. andongensis. Plots were systematically set at
least 200 m apart following the transect lines in the Lama Forest
reserve (100 plots of 50 930 m; Sinasson S, Shackleton, Gl
el
e
Kaka
€
ı, & Sinsin, 2017) and along watercourses in the other forests
(10–30 plots of 30 920 m or 30 930 m).
Within each plot, we sampled and numbered (to avoid confusion
in data collection) Mimusops trees with a dbh (diameter at breast
height) ≥5 cm, and measured their dbh. We then randomly selected
two trees (where applicable) within six dbh classes as follows: C1
(≤10 cm), C2 (10.1–20 cm), C3 (20.1–30 cm), C4 (30.1–40 cm), C5
(40.1–50 cm) and C6 (>50 cm). Every month, we monitored the
flowering and fruiting between March 2014 and April 2015, using
binoculars. We could not collect data during December 2014 and
January 2015, due to site inaccessibility. In total, we monitored 246
trees for M.andongensis (Guineo-Congolian zone) and 175 trees for
M.kummel (152 and 23 in the Guineo-Sudanian and the Sudanian
zones, respectively). We defined the reproductive phenological
events describing changes in the crown of tree as: (i) flower buds, (ii)
flowers present, (iii) immature fruits, (iv) mature but unripe fruits (v)
mature and ripe fruits and (vi) fruits from the previous season pre-
sent (Shackleton, 1999; Vihotogb
e, 2012). We also scored canopy
position (Doucet, 2003) as: (i) dominant (full overhead and side light);
(ii) co-dominant (full overhead light); or (iii) suppressed (no direct
light). However, due to the great height of trees and the intactness
of the vegetation canopy, the observation of the phenophases was
more difficult for large individuals in Lama Forest reserve and pro-
portions of flowering and fruiting trees determined per month
should be seen as conservative.
We obtained monthly values for rainfall, average, minimum and
maximum temperatures for 35 years (1981–2015) from the U.S.
National Climatic Data Center (http://www.ncdc.noaa.gov/) and the
Climate data for cities worldwide (http://en.climate-data.org/).
2.3
|
Data analysis
We analysed differences in flowering and fruiting prevalence
between species and climatic zones, using a Repeated ANOVA with
SINASSON SANNI ET AL.
|
3

two factors; a fixed factor (climatic zone) with three levels and a
repeated factor (monthly observations) with 12 modalities (Menga
et al., 2012). We assessed the variation in the intensity of flowering
and fruiting relative to diameter and canopy position by determining
the proportion of flowering and fruiting trees per diameter classes
and canopy position. We performed Pearson correlations to seek
any relationships between flowering and fruiting intensities, dbh cat-
egory and canopy position. To do so, we transformed the categories
of canopy position into an ordinal variable as follows: (i) for sup-
pressed category, (i) for co-dominant and (iii) for dominant. We then
determined the minimum diameter of maturity (of flowering) and the
minimum diameter of fructification of both species. We also exam-
ined correlations between the monthly percentage of trees in each
phenophase and monthly rainfall, monthly means of average, maxi-
mum and minimum temperatures, using Pearson correlation.
Repeated Measures Analysis was realized in SAS while the other
analyses were carried out using R 3.1.2 (R Development Core Team,
2014).
3
|
RESULTS
3.1
|
Flowering and fruiting according to species
and climatic conditions
Irrespective of species and climatic zones, flowering and fruiting hap-
pened once a year (Figure 3). Flowering started in the dry season
(long dry season in the Guineo-Congolian zone, for M.andongensis)
and concluded during the rainy period (long rainy season in the Gui-
neo-Congolian zone). Fruiting occurred during the rainy season but
started at the beginning of the rainy season in the Guineo-Sudanian
and Sudanian zones (M.kummel), and ended at the beginning of
small dry season in the Guineo-Congolian zone.
FIGURE 1 Location of the study area
and sites
4
|
SINASSON SANNI ET AL.

Similar proportions of the sampled trees flowered in the
three climatic zones (57%, 56% and 61% in the Guineo-Congo-
lian, Guineo-Sudanian and Sudanian zones, respectively). The
appearance of flower buds occurred between February and April
and flowers opened from March to May for M.andongensis (Gui-
neo-Congolian zone). Some buds/opened flowers persisted on
some trees until June. For M.kummel, bud appearance started in
February and ended in April. Flowers opened from March to
May in the Sudanian zone and to June in the Guineo-Sudanian
zone. Flowers/buds persisted on some trees until August. The
peak of flowering was observed in April (beginning of the rainy
season) for both species. However, results showed a significant
difference between climatic zones and species in terms of flow-
ering behaviour of individuals over the observation period
(F
22,267
=8.43, p<.0001).
0
20
40
60
80
100
120
140
160
180
200
220
240
0
5
10
15
20
25
30
35
40
45
50
55
60
65
70
Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr
Precipitations (mm)
Frequency of trees (%)
Months
M. andongensis (Guineo-Congolian zone)
Flowering Fruiting Precipitations (mm)
(A)
(C)
(B)
abc d a
0
20
40
60
80
100
120
140
160
180
200
220
240
0
5
10
15
20
25
30
35
40
45
50
55
60
65
70
Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr
Precipitations (mm)
Frequency of trees (%)
Months
M. kummel (Guineo-Sudanian zone)
Flowering Fruiting Precipitations (mm)
ab
a
b
0
20
40
60
80
100
120
140
160
180
200
220
240
0
5
10
15
20
25
30
35
40
45
50
55
60
65
70
Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr
Precipitations (mm)
Frequency of trees (%)
Months
M. kummel (Sudanian zone)
Flowering Fruiting Precipitations (mm)
ab
a
b
FIGURE 3 Reproductive phenology of Mimusops andongensis (A)
and Mimusops kummel (B and C) during 2014/15; Guineo-Congolian
zone: a: long rainy season, b: short dry season, c: short rainy season,
d: long dry season; Guineo-Sudanian and Sudanian zones: a: rainy
season, b: dry season
0
10
20
30
40
50
60
70
0
50
100
150
200
250
300
Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr
Temperature (°C)
Precipitations (mm)
Months
Guineo-Congolian zone
Precipitations a (mm) Precipitations b (mm)
Temperature a (°C) Temperature b (°C)
0
10
20
30
40
50
60
70
0
50
100
150
200
250
300
Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr
Temperature (°C)
Precipitations (mm)
Months
Sudanian zone
Precipitations a (mm) Precipitations b (mm)
Temperature a (°C) Temperature b (°C)
0
10
20
30
40
50
60
70
0
50
100
150
200
250
300
Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr
Temperature (°C)
Precipitations (mm)
Months
Guineo-Sudanian zone
Precipitations a (mm) Precipitations b (mm)
Temperature a (°C) Temperature b (°C)
FIGURE 2 Monthly rainfall and mean temperature for the study
period (2014/2015) relative to the long-term (1981/2015) means;
Precipitations a and Temperature a: Mean values of precipitations
and temperature for the period 1981/2015; Precipitations b and
Temperature b: Precipitations and temperature for the period 2014/
2015
SINASSON SANNI ET AL.
|
5

Fruiting started about 2 months after the first flower buds
appeared. The formation of fruits started in April while fruit matura-
tion was evident in June for M.andongensis (Guineo-Congolian
zone). In the case of M.kummel, fruit formation started in April in
the Guineo-Sudanian zone and in May in the Sudanian zone, while
the maturation started in June and July in the Guineo-Sudanian and
Sudanian zones, respectively. The peak of fruiting was observed in
June/July (during the most humid period) for both species. There
was a significant difference between climatic zones and species in
terms of fruiting behaviour of individuals over the observation period
(F
22,267
=6.06, p<.0001). The highest per cent of trees (52%) bore
fruits in the Sudanian zone, whilst 7% of trees fruited in the Guineo-
Congolian zone and 20% in the Guineo-Sudanian zone. Similar to
the fruiting, the highest fruit abortion was observed in the Sudanian
zone (39%), 3% in the Guineo-Congolian zone and 8% in the Gui-
neo-Sudanian zone.
3.2
|
Influence of rainfall and temperature
Irrespective of species and climatic zones, there was a positive rela-
tionship between flowering prevalence and temperature (average,
maximum and minimum). There were some variations between the
three climatic zones (between species) in terms of level of significance
of the relationships between the reproductive ability and the different
climatic characteristics. In the Guineo-Congolian zone (M.andongen-
sis), only the relationship between flowering prevalence and tempera-
ture (average, maximal and minimal) was significant. In the two other
climatic zones (M.kummel), flowering was significantly related to mean
and minimal temperatures while for fruiting, the relationship was sig-
nificant with both rainfall (positive) and temperature (negative, with
mean and maximal) but only in the Guineo-Sudanian zone (Table 1).
3.3
|
Influence of diameter and canopy position of
trees
Flowers were observed on almost all diameter classes and fruiting
for trees with dbh >10 cm for M.andongensis, while flowering and
fruiting were observed for all dbh classes for M.kummel. However,
in the Sudanian zone, only trees with dbh <20 cm fruited (Table 2).
In general, the proportion of flowering and fruiting trees increased
with increasing diameter for M.andongensis. For M.kummel, the pro-
portion of flowering increased with increasing diameter in the Gui-
neo-Sudanian zone but this was not the case with the fruiting for
which the highest proportion was obtained for individuals with dbh
10–40 cm. Conversely, in the Sudanian zone, both flowering and
fruiting seemed to decrease with increasing diameter. However,
there was no individual with diameter more than 40 cm in the Suda-
nian zone. The minimum diameter of flowering was 10 cm for M.an-
dongensis and about 6 cm for M.kummel (6 and 6.2 cm in the
Guineo-Sudanian and Sudanian zones, respectively). The minimum
diameter of fructification was 16 cm for M.andongensis, 7 cm in the
Guineo-Sudanian zone and 6.2 cm in the Sudanian zone.
The ability of M.andongensis trees to flower and fruit was influ-
enced by their position in the canopy. The dominant category had the
highest proportion of flowering and fruiting trees, followed by the co-
dominant one. For M.kummel, there was no straight relationship
between tree position in the canopy and the flowering and fruiting
prevalence (Figure 4). However, more dominant trees flowered than
trees in the two other categories but few of them bore fruits. More
co-dominant trees fruited than dominant and suppressed ones. There
was no dominant tree in the Sudanian zone (Table 2) and none of the
existing co-dominant trees flowered or bore fruit.
The results from the Pearson correlation supported the above-
mentioned information about the relationship between the ability of
trees to flower and fruit, and their diameter and canopy position
(Table 3). For M.andongensis, we found strong relationships (r>.9)
between reproductive ability (flowering and fruiting) and tree charac-
teristics (diameter and canopy position), although the relationship
was not significant between fruiting ability and tree position in the
canopy. For M.kummel, relationships between reproductive ability
and tree characteristics were strong (r>.5) but not significant. Also,
only the relationship between flowering ability and tree diameter
was positive. However, there were some differences between the
two climatic zones where the species occurs (Table 3). In the Gui-
neo-Sudanian zone, the relationship between flowering and diameter
was significant, and the relationship with tree position in the canopy
was also positive, while the relationship between fruiting and canopy
position was weak (r<.5). In the Sudanian zone, all the relationships
were strong, negative and nonsignificant.
4
|
DISCUSSION
4.1
|
Phenology across species and climatic
conditions
Irrespective of species, flowering started during the dry season and
ended in the rainy season, while fruiting occurred mostly during the
rainy season. Flowering peaked at the beginning of the rainy season,
and the peak of fruiting was observed during the most humid period.
Moreover, flowering occurred from February to May/June and
TABLE 1 Pearson correlation coefficients between reproductive
ability (flowering and fruiting) and climatic characteristics
Reproductive
ability Rainfall
Average
temperature
Maximal
temperature
Minimal
temperature
Guineo-Congolian zone (Mimusops andongensis)
Flowering 0.2 0.6
a
0.6
a
0.7
a
Fruiting 0.6 0.6 0.6 0.5
Guineo-Sudanian zone (Mimusops kummel)
Flowering 0.2 0.7
a
0.5 0.7
a
Fruiting 0.6
a
0.9
a
0.8
a
0.5
Sudanian zone (M. kummel)
Flowering 0.3 0.7
a
0.5 0.8
a
Fruiting 0.5 0.5 0.6 0.3
a
Significant at 5%.
6
|
SINASSON SANNI ET AL.

fruiting from April till after July, for both species. However, these
two species are found under different climatic conditions and precip-
itation regimes; M.andongensis in the humid and bimodal zone of
the country (Guineo-Congolian zone), while M.kummel occurs in the
subhumid and transition (Guineo-Sudanian) zone and in semi-arid
and unimodal (Sudanian) zone (Adomou, 2010). The difference
TABLE 2 The proportion of flowering
and fruiting trees in the diameter
categories Diameter classes (cm)
Number of trees per canopy position
Flowering (%) Fruiting (%)Dominant Co-dominant Suppressed Total
Guineo-Congolian zone (Mimusops andongensis)
≤10 cm 0 3 34 37 10.8 0.0
10.1–20 cm 1 12 22 45 62.2 3.6
20.1–30 cm 14 16 5 37 70.3 15.4
30.1–40 cm 15 4 1 20 95.0 15.8
40.1–50 cm 8 1 1 10 100.0 30.0
˃50 cm 0 1 0 1 0.0 –
Guineo-Sudanian zone (Mimusops kummel)
≤10 cm 0 2 18 21 47.6 20.0
10.1–20 cm 1 16 30 48 43.7 42.9
20.1–30 cm 5 17 20 42 76.2 37.5
30.1–40 cm 7 5 8 20 80.0 56.2
40.1–50 cm 3 0 2 5 80.0 0.0
˃50 cm 14 2 0 16 93.7 33.3
Sudanian zone (M. kummel)
≤10 cm 0 0 3 3 66.7 100.0
10.1–20 cm 0 0 6 10 60.0 100.0
20.1–30 cm 0 2 2 4 50.0 0.0
30.1–40 cm 0 0 1 1 0.0 –
40.1–50 cm 0 0 0 0 ––
˃50 cm 0 0 0 0 ––
0
10
20
30
40
50
60
70
80
90
100
Suppressed Co-dominant Dominant
Frequency of trees (%)
Canopy position of trees
Guineo-Congolian zone
Flowering Fruiting
0
10
20
30
40
50
60
70
80
90
100
Suppressed Co-dominant Dominant
Frequency of trees (%)
Canopy position of trees
Guineo-Sudanian zone
Flowering Fruiting
0
10
20
30
40
50
60
70
80
90
100
Suppressed Co-dominant Dominant
Frequency of trees (%)
Canopy position of trees
Sudanian zone
Flowering Fruiting
(a) (b)
(c)
FIGURE 4 Reproductive phenology of
Mimusops andongensis (a) and Mimusops
kummel (b and c) according to canopy
position of trees
SINASSON SANNI ET AL.
|
7

between the climatic zones is also confirmed by the climatic/humid-
ity index of Mangenot (a better measure of climatic conditions than
annual rainfall) which decreases from the Guineo-Congolian to Suda-
nian zone (Adomou et al., 2006). The two study species displayed
similar periods of flowering and fruiting. These results indicated that
the species phenology may be strongly shaped by phylogenetic
membership. Wright and Calderon (1995) and Lobo et al. (2003) sug-
gested that plant phenology can be strongly restricted by phyloge-
netic membership or life form. Phylogenetic restrictions may shape
plant phenology more than any local drivers, and species of the same
taxa should display similar phenological patterns independently of
their geographical location (Davies et al., 2013). Nonetheless, there
was a significant difference between the species according to indi-
vidual reproductive behaviour over both the flowering and fruiting
periods. Also, in each climatic zone or for each species, the sampled
trees did not flower or bear fruits at the same time (Fernandez Otar-
ola et al., 2013).
Our results showed that M.andongensis and M.kummel flower
between February and May/June and fruit from April until after July.
Previous work on melliferous plants around Manigri district in the
Guineo-Sudanian zone of Benin mentioned that M.kummel individu-
als bear flowers in March and April (Yedomonhan, Tossou, Akoegni-
nou, Demenou, & Traore, 2009). In the Analytical Flora of Benin,
flowers have been mentioned to occur in April and fruits in Septem-
ber and October (Ako
egninou, van der Burg, & van der Maesen,
2006). For M.andongensis, fruit harvesting during the short dry sea-
son (mid-July to mid-September) has been reported by local people
in Benin (Boedecker, Termote, Assogbadjo, van Damme, & Lachat,
2014), while fruits were seen in August and September in the
Dzanga-Sangha Reserve in Congo (Harris, 2002). However, flowers
have also been mentioned in Benin in January for M.kummel
(Ako
egninou et al., 2006), while in Ethiopia, flowers were observed
between January and June, and fruits between April and December
(Chikamai et al., 2006). Mimusops andongensis flowering was
reported in January and fruiting between November and April in
Guinea-Bissau (Catarino, Martins, Pinto Basto, & Diniz, 2008). More-
over, according to local people around Lama Forest reserve,
flowering sometimes occurs twice a year for M.andongensis, mean-
ing that trees may flower in groups. Previous studies have shown
the reproductive phenology to be biannual for some species (Menga
et al., 2012). There may be interannual variation in flowering and
fruiting periods in relation to shifts in climatic drivers (Lobo et al.,
2003). Also, due to the height of some trees and the fact that the
canopy is very closed in some parts of Lama Forest reserve, the
observation of phenological events was sometimes difficult. Thus,
long-term observations using appropriate tools will help for better
description of phenology patterns of the study species.
We observed total flower abortion for some trees and immature
fruits abortion for others, in both species. Flower abortion may be
linked to limitation in the availability of pollen and pollinators, and
hence pollination failure, while the main cause of failure in fruit pro-
duction and fruit abortion is an insufficiency of resources (Bawa &
Webb, 1984; Pearse, Koenig, Funk, & Pesendorfer, 2015; Straka &
Starzomski, 2014). However, previous studies have highlighted that
the number of flowers and fruits, as well as their position in the
inflorescence, may influence pollen flow, pollinator attraction and
resource allocation (Bawa & Webb, 1984; Stephenson, 1981). More-
over, it is a common pattern in many plants, especially hermaphrodi-
tic species, to have excessive flowering and that mature fruits are
produced from only a small portion of the available flowers; thus,
there is frequent abortion of flowers and immature fruits (Bawa &
Webb, 1984; Stephenson, 1981). Furthermore, any factors (environ-
mental stresses) that affect tree health can also affect fruit set and
retention (Nyoka, Sileshi, & Silim, 2015). Understanding patterns of
fruit production in relation to environmental drivers may therefore
contribute in predicting demographic dynamics of flowering plant
species (Straka & Starzomski, 2014).
4.2
|
Phenological patterns in relation to
temperature and rainfall
Flowering started in the dry season and concluded at the beginning of
the rainy season, while fruiting occurred during the rainy season, for
both species. This mirrors the pattern of many tropical species which
bear fruits during the wet season when water availability is not limiting
(Polansky & Boesch, 2013). This suggests that the species phenology
is linked to climatic conditions. Climate is a common driver of plant
phenology (Wolkovich et al., 2014) as was found in this study. For
instance, flowering was positively correlated with temperature, irre-
spective of species and climatic zones. Conversely, fruiting was nega-
tively linked to temperature while positively correlated with rainfall, in
the Guineo-Sudanian zone. Our results supported the assumption that
temperature and rainfall are important determinants of flowering and
fruiting (Crimmins et al., 2011; Morellato et al., 2013).
Global warming is increasing the temperature and consequently
may impact species by disrupting the timing of their reproductive
phenology (Morellato et al., 2016). In West Africa, for instance, pre-
dictions have shown that temperature may increase by up to 2°Cby
2050 (Konare, 2010). We found flowering prevalence of M.andon-
gensis and M.kummel to be positively related to temperature and,
TABLE 3 Pearson correlation coefficients between reproductive
ability (flowering and fruiting) and tree characteristics (diameter and
position in canopy)
Reproductive ability Diameter Position in canopy
Guineo-Congolian zone (Mimusops andongensis)
Flowering 0.92
a
1.00
a
Fruiting 0.97
a
0.97
Guineo-Sudanian zone (Mimusops kummel)
Flowering 0.92
a
0.71
Fruiting 0.16 0.54
Sudanian zone (M. kummel)
Flowering 0.96 0.87
Fruiting 0.90 0.87
a
Significant at 5%.
8
|
SINASSON SANNI ET AL.

therefore, warmer temperatures may shift flowering, perhaps flower-
ing earlier in the year. If the species change their flowering time or
flower earlier, pollination success might be diminished because the
pollinators may not yet be ready, especially if there is synchroniza-
tion between tree and pollinator development (Carstensen, Sabatino,
Trøjelsgaard, & Morellato, 2014). Furthermore, fruiting in M.kummel
in the Guineo-Sudanian zone was negatively correlated with temper-
ature and positively with rainfall, and fruit maturity occurred during
rainy season. Thus, if the mentioned relationship of fruiting with
temperature and rainfall occurs in all the climatic zones, any increase
in drought frequency (warmer periods over the year) and tempera-
ture might cause failures in fruit production and increase fruit abor-
tion. This could have negative impacts on frugivorous birds and
animals that depend on the species fruits (Kagoro-Rugunda & Hashi-
moto, 2015). However, phenology is often an adaptive characteristic
and many plant species can adjust their phenological patterns in rela-
tion to changes in different drivers (Colautti, Eckert, & Barrett,
2010). Nonetheless, climatic change should be considered as a seri-
ous threat to species phenology and consequently species survival
(Wolkovich et al., 2014). Some studies recommend that phenology
be integrated in modelling of suitable ecological habitats under cli-
mate change (Rosemartin et al., 2014). Although not considered in
this study, soil properties such as moisture and nutrients (Wolkovich
et al., 2014), and topography (Hindle, Kerr, Richards, & Willis, 2015)
are important drivers that should be considered for further long-term
investigations of environmental drivers of the species phenology.
4.3
|
Phenological relationships with tree diameter
and position in the canopy
This study showed that the prevalence of flowering and fruiting of
M. andongensis was positively related to tree diameter, suggesting
that the bigger the tree, the greater its ability to flower and bear
fruits. For M. kummel, only flowering ability was positively linked to
tree diameter and significant in the Guineo-Sudanian zone; the rela-
tionship with fruiting was negative but not significant. For some
tropical species, the ability to flower and bear fruit increases as
diameter increases, but this relationship between tree diameter and
reproductive ability might be shifted by other environmental drivers
of flower and fruit production (Plumptre, 1995). However, flowering
ability of M.kummel in the Sudanian zone was negatively correlated
with tree diameter. This might be because that climatic zone is char-
acterized by small diameter trees (Adomou et al., 2006) and that the
biggest individuals are old.
For M.andongensis, we found a positive correlation between
reproductive phenology and tree position in the canopy, suggesting
that the higher the tree, the greater its ability to flower and bear
fruits. Plant phenology is also affected by irradiance/photoperiod
(Morellato et al., 2013) which at the individual level depends on the
position of a tree in the canopy, especially in dense forests where
the canopy is closed. In the “Noyau central”of Lama Forest reserve
where the phenology of M.andongensis was monitored, the vegeta-
tion is dense, and the canopy is mostly closed, but with open areas
due to past land use changes (Djego & Sinsin, 2007). Conversely, the
flowering and fruiting abilities of M.kummel were negatively corre-
lated with tree position in the canopy, and the relationship was not
significant. The canopy of the forests where M.kummel occurs was
more open relative to Lama Forest reserve (Pers. Observ.), indicating
that sunlight accessibility to trees may not be a limiting factor in
those forests. This might explain the negative and nonsignificant
relationship between reproductive phenology of M.kummel and tree
position in canopy. Our results thus highlighted that plant phenology
is also influenced by canopy openness. However, the relationship
between flowering and tree position in the canopy was positive in
the Guineo-Sudanian zone. These results confirmed that the repro-
ductive phenology of the species is linked to other environmental
factors (e.g. climate) that might influence the relationship between
the species phenology and tree position in the canopy.
5
|
CONCLUSION
This study has indicated that, although flowering and fruiting of
both species were linked to climatic conditions (temperature and
rainfall), phylogenetic membership is an important factor constrain-
ing their reproductive phenology. Nonetheless, the reproductive
phenology is strongly correlated with climatic conditions and conse-
quently any shifts in the climate might affect species populations
as well as other dependent organisms and services. However,
because of the relatively short length of this study, further work
across multiple years is required. Other factors also contributed to
the observed trends. For instance, tree diameter and canopy posi-
tion are important physiological characteristics that influence spe-
cies phenology. Further long-term phenological investigations using
appropriate tools and including soil moisture and nutrients and
topography are needed for highlighting the phenological patterns of
both species in relation to environmental drivers (Morellato et al.,
2013). Also, though quite complex, a mixed model considering both
biotic and abiotic drivers may give a better understanding of phe-
nological patterns in relation to the different drivers (Wolkovich
et al., 2014). Another important research axis is the investigation of
the quantity of flowers and fruits produced in relation to tree
diameter and canopy position.
ACKNOWLEDGEMENTS
We thank Micha€
el Hounsa, Christian Affoukou, Herv
e Kanlissou and
Cyrus Binassoua for field assistance. Thanks go also to the Interna-
tional Foundation for Science (IFS, grant D/5467-1 to KGSS), OWSD
(Organization for Women in Science for the Developing World) and
SIDA (Swedish International Development Cooperation Agency), for
financial support.
COMPETING INTERESTS
The authors declare that they have no competing interests.
SINASSON SANNI ET AL.
|
9

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How to cite this article: Sinasson Sanni GK, Shackleton CM,
Sinsin B. Reproductive phenology of two Mimusops species in
relation to climate, tree diameter and canopy position in
Benin (West Africa). Afr J Ecol. 2017;00:1–11. https://doi.org/
10.1111/aje.12457
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