Vol. 16(9), pp. 1278-1288, September, 2020
DOI: 10.5897/AJAR2020.14730
Article Number: 153987064843
ISSN: 1991-637X
Copyright ©2020
Author(s) retain the copyright of this article
http://www.academicjournals.org/AJAR
African Journal of Agricultural
Research
Full Length Research Paper
Floral activity of Apis mellifera (Hymenoptera: Apidae)
on Bidens steppia (Asteraceae), Cordia africana
(Boraginaceae), Pittosporum viridiflorum
(Pittosporaceae) and Psychotria mahonii (Rubiaceae) in
Nyambaka (Adamawa, Cameroon)
Nentcherse Mbere1,2*, Michelson Azo’o Ela3, Tchobsala2,4 and Fernand-Nestor
Tchuenguem Fohouo1
1
Department of Biological Sciences, Laboratory of Applied Zoology, University of Ngaoundere. P. O. Box 454
Ngaoundere, Cameroon.
2
Department of Biological Sciences, Laboratory of Biodiversity and Sustainable Development, University of Ngaoundere.
P. O. Box 454 Ngaoundere Cameroon.
3
Department of Biological Sciences, Laboratory of Entomology, University of Maroua, P. O. Box 814 Maroua Cameroon.
4
Department of Biological Sciences, Laboratory of Botany, University of Maroua, P. O. Box 814 Maroua Cameroon.
Received 20 January, 2020; Accepted 2 April, 2020
Experiments were conducted at Nyambaka in the Adamawa Region of Cameroon, from March 2017 to
November 2018, for assessing the apicultural potential of Bidens steppia, Cordia africana, Pittosporum
viridiflorum and Psychotria mahonii. In order to improve the beekeeping productivity, it is important to
investigate the diversity of bee plants in a given apiary site. To that end, the foraging behaviour of Apis
mellifera workers was studied on the flowers of each plant species twice a week during the whole
blooming period. The abundance of opened flowers per plant, floral products harvested by foragers,
mean duration of floral visit, mean density of foragers, sugar content of nectar of each plant species,
and number of effective visits of A. mellifera on flowers were assessed. Results indicated that,
honeybee workers harvested nectar of each plant species; B. steppia and P. viridiflorum were intensely
foraged for pollen harvesting too. The abundance of workers/1000 flowers varied from 123 on P.
mahonii to 724 on C. africana. The mean value of the sugar content of nectar oscillated from 19.50% (C.
africana) to 38% (B. steppia). C. africana and P. mahonii were highly nectariferous plant species while
B. steppia was very highly polliniferous and slightly nectariferous and P. viridiflorum very highly
nectariferous and slightly polliniferous. During its foraging activity, workers improved the pollination
possibilities of plant species. By planting or protecting these plant species, a bee-friendly garden can
be preserve for providing nectar flow and pollen availability for beekeeping purpose.
Key words: Apiary, apicultural value, beekeeping, bee plant, foraging behaviour, sugar content.
INTRODUCTION
Beekeeping is one of the most important cultural and
economic activities in the Adamawa region of Cameroon
(Ingram, 2011). The highest quantity of honey consumed
or marketed in this country is from this region which has a
Mbere et al.
suitable climatic condition for the proliferation of
honeybees (INADES, 2000). Despite the favorable agroecology of honey production and the high number of bee
colonies this region is endowed with, the honey
production and productivity level in Cameroon is still very
low (Dongock et al., 2017). Yet, sustainable beekeeping
can be improved through the understanding and
conservation of plants producing nutrient for the
honeybees mainly in terms of nectar and pollen (El-Nebir
and Talaat, 2013).
Apis mellifera is one of the bees raised on a large scale
in beekeeping to produce honey and for pollination. This
species comprises 28 subspecies including Apis mellifera
adansonii, which has its origin from Africa (Fletcher,
1978). Honeybee workers are attracted commonly to
plants that produce nectar and pollen. Nectar is a sweet
substance that attracts bees which also need pollen in
their diet (Louveaux, 1984). These food sources provide
the nutritional requirements of the bee colonies. Nectar
as a source of honey provides heat and energy while
pollen provides protein, vitamins and fatty substances
(Amsalu et al., 2003). During floral visits for nectar
harvesting and pollen gathering, honeybees, in turn,
pollinate plants; thus they can help in boosting fruit and
seed yields of the host plant and then propagate their
species (Klein et al., 2007; Allsopp et al., 2008).
The honey and other products of honeybees depend on
the availability of floral resources in a given area (Amsalu
et al., 2003). Intending to improve the level of honey
production both in quantity and quality in the Adamawa
region of Cameroon, several findings are available in
enhancing beekeeping practice regarding the inventory of
bee plants in some sites like Ngaoundere (Tchuenguem
et al., 2010; Ingram, 2011; Djonwangwé et al., 2011;
Egono et al., 2018; Wékéré et al., 2018) and Ngaoundal
(Dongock et al., 2017).
Nyambaka is a small locality in the Adamawa region of
Cameroon where beekeeping is still done on a smallscale. In this area, beekeeping practice appears like a
commercial enterprise; it offers not only diverse hive
products which can be sold in local markets and become
an important source of regular income for farmer families,
but also provide complementary services, such as plant
pollination. Moreover, locally, bee products improve farm
family nutrition and can provide traditional health care
remedies. There are many plant species that produce a
large amount of nectar and pollen for bees to be collected
in the locality. Some of these plants are important as they
provide bees with a surplus of honey. Small-scale
beekeeping is considered as an important occupation
that contributes significantly to livelihood security in that
region. Yet, most of the honey is produced with traditional
1279
hives consisting of bast and grass; besides, bee plants
are not yet well known by beekeepers in this area. It is,
therefore, an important practice to help bees in their
survival by adding to the shrinking inventory of flower-rich
habitat in the study locality.
The United Nations World Health Organization
estimates that as many as 5.6 billion people, 80% of the
world population, utilize herbal medicine for primary
health care (Shen et al., 2012). Bidens steppia (Steetz)
Sherff
(Asteraceae),
Cordia
africana
Lam.
(Boraginaceae),
Pittosporum
viridiflorum
Sims
(Pittosporaceae), and Psychotria mahonii C.H. Wright
(Rubiaceae) are four multipurpose plant species which
are often harvested for local use as food and medicine in
Nyambaka. In the locality, different preparations of parts
of B. steppia plant are commonly purported to treat
several categories of illnesses such as diabetes and
malaria. In the literature, extracts of B. steppia have
antitumor (Sundararajan et al., 2006), anti-inflammatory,
antimicrobial (Pereira et al., 1999), antidiabetic,
antimalarial (Tobinaga et al., 2009) properties. C.
africana is used as firewood. The fruit pulp of this plant is
edible and is added as a sweetener to food. The leaves
serve as fodder for livestock. Leaf decoctions are
administered to treat headache, nose bleeding, dizziness
and vomiting during pregnancy, wounds and worms while
root decoctions are drunk to treat jaundice (Obeng,
2010). The categories to which P. viridiflorum is used in
traditional medicine include wounds, treatment of
veterinary ailments, gastrointestinal tract and sexually
transmitted diseases, circulatory and inflammatory
disorders, as well as diseases such as cancer,
tuberculosis, and malaria (Madikizela and McGaw, 2017).
As for P. mahonii, fresh rhizomes are chewed and the
juice swallowed to treat intestinal tract diseases and
worms.
In addition to their medicinal importance, all four plant
species studied have flowers that produce nectar and
pollen available for bee species. It is well known in the
literature that the productivity of the honeybee colonies is
proportional both to the abundance and attractiveness of
the nectariferous and polliniferous plants present in the
environment of the apiary (Williams and Carreck, 1994;
Van’t et al., 2005). Thus, sustainable beekeeping in a
given region requires detailed knowledge of the
apicultural value of plant species that grow there for their
optimal management (Dongock et al., 2017). Moreover,
honeybee being a bio-indicator species (Porrini et al.,
2003), medicinal plants are an interesting source for the
production of honey with medicinal biological activity very
close to their floral origin (Liberato et al., 2011). That is
why it is interesting to associate a crop of medicinal
*Corresponding author. E-mail: nentchersembere@gmail.com. Tel. (+237) 699 91 11 08.
Author(s) agree that this article remain permanently open access under the terms of the Creative Commons Attribution
License 4.0 International License
1280
Afr. J. Agric. Res.
plants with beekeeping. However, there is no available
data published on the relationships between African
honeybees and many local and medicinal plant species
including B. steppia, C. africana, P. viridiflorum and P.
mahonii in Cameroon. The main objective of the present
research work was to determine the apicultural status of
these plant species in Nyambaka, to improve the
beekeeping potential and enhance the value of the plants
studied in this locality. For each plant species, we
recorded the foraging activity of A. mellifera on flowers
and estimated its apicultural value.
MATERIALS AND METHODS
Study site and biological material
The present study was carried out from March 2017 to November
2018 in Nyambaka, a village located in the South of Ngaoundere,
the capital of the Adamawa region of Cameroon. This region is
located between the 6th and 8th degrees of latitude north and
between the 11th and 15th degrees of longitude east; it belongs to
the high-altitude Guinean Savannah agro-ecological zone (Djoufack
et al., 2012). The climate is characterized by a rainy season (April
to October) and a dry season (November to March), with an annual
rainfall of approximately 1500 mm, a mean annual temperature of
22°C, and a mean annual relative humidity of 70% (Amougou et al.,
2015) which are suitable climatic conditions for the beekeeping
practice. Plants chosen for observations were located in an area of
1.5 km in diameter, centered on a Kenyan top-bar hive of A.
mellifera colony. The hive was located at the following coordinates:
6°89’62’943’N, 14°09’28’038’E, 1136 m a.s.l.
The animal material included many insect species naturally
present in the environment. The number of honeybee colonies
located in the area varied from 60 in March 2017 to 69 in November
2017 and from 42 in March 2018 to 72 in November 2018. Apart
from the honeybee colonies located in the experimental site, other
colonies around the experimental site have not been inventoried
since the radius action of foragers may exceed 12 km around the
hive (Louveaux, 1984). The vegetation was represented in the
study site by crops, ornamental plants, hedge plants and native
plants of savannah and gallery forests.
counted on these flowers at a given time x (Tchuenguem et al.,
2004). The disruption of the activity of foragers by competitors and
the attractiveness exerted by other plant species on A. mellifera
was assessed by direct observations.
Evaluation of the sugar content of the nectar of different plant
species
The concentration in total sugar of the nectar is an important
parameter for the attractiveness of the honeybee concerning many
flowers (Philippe, 1991). This parameter was determined with a
handheld refractometer (0-90% Brix) and a thermometer that gave
the ambient temperature, from March 2017 to November 2018. A.
mellifera workers in full activity of nectar harvesting were captured
on flowers and anesthetized by introducing them in a small jar
containing cotton moistened with chloroform. The nectar was then
removed from honeybee crop by exerting pressure on the bee
abdomen placed between the thumb and the forefinger of the
experiment; the nectar in the mouth was then expelled and its
concentration in total sugars measured in g/100 dry matter
(Tchuenguem et al., 2007). The registered values obtained were
corrected according to the ambient temperature, using a table
provided by the device leaflet (Cruden and Hermann, 1983).
Evaluation of the apicultural value of different plant species
As for other plant species, the apicultural value of each plant
species studied was assessed using data on the flowering intensity,
the degree of attractiveness of A. mellifera workers to nectar and/or
pollen (Villières, 1987; Népidé et al., 2016).
Evaluation of the influence of Apis mellifera on pollination
To evaluate the ability of A. mellifera to act as a pollinator of each
plant species during the nectar harvesting, the number of time a
forager came into contact with the stigma of the visited flower was
noted (Freitas, 1997). This approach allows highlighting the
involvement of A. mellifera in self-pollination and cross-pollination
(Zumba et al., 2013; Potts et al., 2015).
Statistical analysis
Study of the foraging activity of A. mellifera on flowers
From March 2017 to November 2018, the foraging behaviour of A.
mellifera workers was recorded on flowers of different plant species.
Data were registered twice a week, between 07:00 a.m. and 06:00
p.m., at three-time intervals per day: 07:00-11:00 a.m., 11:00 a.m.03:00 pm and 03:00-06:00 p.m. For any plant species visited by the
honeybee browsers and for each investigation date, the following
parameters were registered for each time frame and, whenever
possible: the number of effective visits (the bee came into contact
with the stigma) (Jacob-Remacle, 1989; Freitas, 1997), the mean
duration of visits using a stopwatch (Tchuenguem et al., 2004). The
density of foragers (highest number of individuals foraging
simultaneously on a flower or 1000 flowers) was also assessed.
The density of foragers was recorded following the direct counting
on the same dates and daily periods as for the registration of the
duration of individual flower visits; for this purpose, some foragers
were counted on a known number of flowers. The density of
foragers per 1000 flowers (A1000) was then calculated using the
following formula: A1000 = ((Ax/Fx)*1000) where Fx and Ax are the
numbers of opened flowers and the number of foragers effectively
Data were subjected to descriptive statistics using SPSS 16. The
Student’s t-test was used for the comparison of means between two
samples and Chi-square (χ2) for the comparison of two
percentages. The analysis of variance (ANOVA) was used for multicomparison of means.
RESULTS
Characteristics of the plant species studied
Tables 1 and 2 described plant species studied and the
relative abundance of opened flowers per month for each
of these plant species during both observation years. It is
indicated from these tables that apart from C. africana
which is mainly cultivated in the locality for the fruit
production and shady purposes, B. steppia, P.
viridiflorum and P. mahonii are respectively a shrub and
small trees which grow spontaneously in the savannah.
Mbere et al.
1281
Table 1. Scientific name, botanic family, biotope, some characteristics and strength of different plants studied.
Scientific name and status
Family
Biotope
Flowering period
DCOF
Bidens steppia (++; sh)
Cordia africana (+; tr)
Pittosporum viridiflorum (++; tr)
Psychotria mahonii (++; tr)
Asteraceae
Boraginaceae
Pittosporaceae
Rubiaceae
Savannah
Garden
Savannah
Savannah
June-November
June-September
March-June
March-July
Yellow-orange
White
Greenish-white
White
Number of plants
2017
2018
3634
4275
23
25
764
716
527
585
+: cultivated plant; ++: spontaneous plant; tr: tree; sh: shrub; DCOF: dominant colour of flowers.
Table 2. Relative abundance of opened flowers on each plant species per month during the two investigation periods.
Plant species
Bidens steppia
Cordia africana
Pittosporum viridiflorum
Psychotria mahonii
M
A
*
**
***
****
March 2017 to November 2017
J
Ju
Au
S
*
**
****
**
****
****
**
****
**
***
**
*
Ma
O
****
*
N
**
M
A
*
**
***
***
March 2018 to November 2018
Ma
J
Ju
Au
S
*
**
**
***
*
****
***
**
****
**
****
**
*
O
****
*
N
**
M : March ; A : April ; Ma : May ; J : June ; Ju : July ; Au : August ; S : September ; O : October ; N : November ; *: ≤100 flowers = rare; ** : ˃100 and ≤500 flowers = little abundant; ***: ˃500 and ≤1000
flowers = abundant; ****: ˃1000 flowers = very abundant.
The color of the flowers of these plant species
varied from orange-yellow, greenish-white and
white respectively for B. steppia, P. viridiflorum, C.
africana and P. mahonii. Furthermore, the number
of these plant species varied from about 25 for C.
africana to about 4275 for B. steppia. These
important numbers of plant species in the studied
area enabled the availability of a large amount of
floral mass during their blossoming.
A. mellifera foraging activity on flowers
Floral products harvested, intensity and
frequency of collection of different products
The identity of the food harvested by A. mellifera
workers from the flowers of each plant species
investigated and the intensity and frequency of the
collection of different food resources are
presented in Table 3. The main results from this
table indicated that: (a) B. steppia was weakly
visited for nectar gathering while its pollen was
highly attractive for A. mellifera workers (b) P.
viridiflorum was slightly visited for its pollen while
its nectar was abundantly harvested by honeybee
foragers; (c) C. africana and P. mahonii were only
visited for supplying nectar needs of A. mellifera
as their pollen was scarcely collected. In general,
the intensity of nectar or pollen collection varied
with plant species and for a given plant species
with the time.
The distribution of
nutritive substances
harvested by A. mellifera on flowers in terms of
nectar and/or pollen of a given plant species
according to each observation time interval is
reported in Table 4. A. mellifera workers foraged
nectar and/or pollen of B. steppia, C. africana, P.
viridiflorum and P. mahonii almost during the
whole daily period, from 06:00 a.m. till 06:00 p.m.
and during all the blooming period of each plant
species studied. This is an illustration that these
plant species are important and abundant sources
of nutrients for A. mellifera.
Density of foragers
The values of the density of foragers are reported
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Afr. J. Agric. Res.
Table 3. Floral products harvested by A. mellifera from the flowers of plants according to period, harvesting intensity and abundance of food.
Variation of food harvesting according to the time period
Plant
species
B. steppia
C. africana
P. viridiflorum
P. mahonii
March to November 2017
M
A
2
3
N
N2
N
N4
Ma
J
4
N1
N4P1
N2
1
NP
N3
Ju
P1
N4
Au
N1P2
N3
1
N
March to November 2018
S
N2P4
N2
O
N2P4
N1
N
P2
M
A
Ma
N1
N1
N3P1
N3
N4P2
N4
J
P1
N1
N4P1
N2
Ju
P2
N4
Au
N1P2
N3
S
N2P4
N3
O
N2P4
N1
N1
N
P2
Seasonal frequency of food
harvesting
TD nDN
pDN
nDP
pDP
96
32
33%
100 100%
64
64
100%
64
64
100%
32
40%
80
80
100%
-
M: March; A: April; Ma: May; J: June; Ju: July; Au: August; S: September; O: October; N: November; TD: Total number of observation days; nDN: number of days where the collection of nectar was
effective; pDN: percentage of days were the collection of nectar was effective; nDP: number of days where the collection of pollen was effective; pDP: percentage of days where the collection of pollen
was effective; N: Nectar; P: Pollen; 1, 2, 3 and 4 given as superscripts indicate the harvesting intensity which was very low, low, high and very high respectively.
Table 4. Products harvested by Apis mellifera from the flowers of the four plants species according to daily time interval.
Daily time interval
07.00 - 11.00 am
Pollen and nectar
Nectar
Nectar and pollen
Nectar
Plant species
Bidens steppia
Cordia africana
Pittosporum viridiflorum
Psychotria mahonii
11.00 am - 3.00 pm
pollen
Nectar
Nectar
Nectar
3.00 - 6.00 pm
Pollen and nectar
Nectar
Nectar and pollen
Nectar
Table 5. Abundance of Apis mellifera workers per 1000 flowers according to plant species and months.
Plant species
Bidens steppia
Cordia africana
Pittosporum viridiflorum
Psychotria mahonii
M
A
5
13
462
521
March 2017 to November 2017
Ma
J
Ju
Au
S
4
69
413
18
504
724
107
607
26
193
94
17
O
571
7
N
26
M
A
17
7
362
123
March 2018 to November 2018
Ma
J
Ju
Au
S
1
13
102
541
6
430
643
132
702
10
684
231
21
O
552
13
N
13
M : March ; A : April ; Ma : May ; J : June ; Ju: July ; Au : august ; S : September ; O : October ; N : November.
in Table 5. The highest number of A. mellifera
workers foraging simultaneously per flower was
one for each plant species. The mean abundance
per 1000 flowers in 2017 was 216 (n = 240; s =
122; maximum = 517) on B. steppia, 272 (n = 197;
s = 143; maximum = 727) on C. africana,
Mbere et al.
1283
Table 6. Duration of Apis mellifera visits on flowers of the four plants species according to the study periods and harvested products.
Plant species
Bidens steppia (N)
Bidens steppia (P)
Cordia africana (N)
Pittosporum viridiflorum (N)
Pittosporum viridiflorum (P)
Psychotria mahonii (N)
n
205
245
253
234
97
552
March-November 2017
Mean duration of visit (sec)
m ± sd
mini
5.27 ± 2.73a
1
6.42 ± 3.86b
2
5.03 ± 2.21a
2
c
3.92 ± 2.66
1
3.54 ± 2.48c
1
4.48 ± 1.92ac
1
maxi
16
21
15
15
12
11
n
241
451
306
237
106
172
March-November 2018
Mean duration of visit (sec)
m ± sd
mini
maxi
5.14 ± 2.53a
1
12
6.14 ± 5.24b
1
13
5.28 ± 2.04a
2
14
c
3.88 ± 2.49
1
12
4.10 ± 2.16c
1
11
4.55 ±1.91ac
2
12
Comparison of means of the two
study periods
t- value
0.52
0.73
1.39
0.17
1.72
0.42
df
444
694
557
469
201
722
p- value
˃ 0.05NS
˃ 0.05NS
˃ 0.05NS
˃ 0.05NS
˃ 0.01NS
˃ 0.05NS
n: sample size; m: mean; mini: minimum; maxi: maximum; N: Nectar collection visits; P: Pollen collection visits; sd = standard deviation ; NS = Non significant. Mean values in the same column
(mean duration of a bee visit for nectar or pollen harvesting as a function of a given plant species) or in the same line (for a given plant species as function of the floral product harvested and the year)
but with different letters vary significantly (P < 0.05).
271 (n = 146; s = 131; maximum = 643) on P.
viridiflorum and 167 (n = 205; s = 94; maximum =
727) on P. mahonii. In 2018, the corresponding
figures was 203 (n = 268; s = 118; maximum =
552) on B. steppia, 244 (n = 217; s = 128;
maximum = 643) on C. africana, 272 (n = 116; s =
142; maximum = 702) on P. viridiflorum and 213
(n = 189; s = 121; maximum = 684) on P. mahonii.
The optimal value of the density of A. mellifera
workers corresponded with the month of the peak
of blossoming of each plant species studied which
are: September and October for B. steppia, July to
August for C. africana, April and May for P.
viridiflorum and P. mahonii respectively. The
difference of the mean density of foragers was not
significant for each plant species according to the
year.
Duration of visits
Results from Table 6 highlighted the variation of
the mean duration of A. mellifera visit as a
function of the floral product harvested and for a
given plant species according to the year. As
pollen grains of C. africana and P. mahonii were
not so interesting for foragers, only the mean
duration of a visit for pollen collection by A.
mellifera on B. steppia and P. viridiflorum were
registered in both years. Overall, the duration of a
forager visit varied with the floral product
searched for and for a given product with the host
plant species studied. The difference was
significant between pollen and nectar gathering on
B. steppia in 2017 (t = 5.23; df = 448; P < 0.05)
and 2018 (t = 3.97; df = 690; P < 0.05), between
nectar collection among plant species in 2017 (F =
6.52; df = 3, 1240; P < 0.05) and 2018 (F =5.93;
df = 3, 952; P < 0.05) and between pollen
collection on B. steppia and P. viridiflorum in 2017
(t = 7.63; df = 340; P < 0.05) and 2018 (t = 6.57;
df = 555; P < 0.05). Workers of A. mellifera were
disturbed during their foraging activity by other
flower-visiting insects or abiotic parameters such
as the wind and the rainfall. Some disturbances
have resulted in the interruption of some
honeybee visits and consequently reduced the
time spend on the corresponding flower, thus
obliged foragers to move swiftly from flower to
flower.
Influence of neighboring flora
During the observation periods of each of the four
plant species under investigation, flowers of many
other plant species growing in the study area were
visited by A. mellifera for nectar (ne) and/or pollen
(po). Among these plants were, Manihot esculenta
(Euphorbiaceae:
ne),
Tithonia
diversifolia
(Asteraceae: ne), Bidens pilosa (Asteraceae: ne +
po), Stylosanthes guianensis (Fabaceae: ne +
po), Hibiscus rosa-sinensis (Malvaceae: ne + po),
Sida rhombifolia (Malvaceae: ne + po), Terminalia
schimperiana (Combretaceae: ne + po),
Terminalia macroptera (Combretaceae: ne + po),
Sesbania pachycarpa (Fabaceae : ne + po),
Mimosa invisa (Mimosaceae: po), Mimosa pudica
(Mimosaceae:
po),
Senna
mimosoides
(Fabaceae: po), and Zea mays (Poaceae: po).
During one foraging trip, a forager was not
observed moving from the flowers of a given plant
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Afr. J. Agric. Res.
Table 7. Concentration in total sugar of the nectar of plant species studied.
Concentration in total sugar of the nectar (%)
Plant species
Bidens steppia
Cordia africana
Pittosporum viridiflorum
Psychotria mahonii
March 2017 to November 2017
n
62
60
46
37
m±s
38.07 ± 9.60a
19.43 ± 3.42b
29.54 ± 6.63c
26.03 ± 1.03c
mini
22
10
21
23
maxi
47
21
36
27
March 2018 to November 2018
n
45
73
69
43
m±s
36.29 ± 9.69a
19.05 ± 3.25b
28.84 ± 6.14c
25.97 ± 0.96c
mini
23
10
21
23
maxi
46
22
34
27
Comparison of means
of the two study periods
t
ddl
P
0.94
105
> 0.05NS
0.65
131
> 0.05NS
0.58
113
> 0.05NS
0.26
78
> 0.05NS
Mean values in the same column (plant species) or in the same line (for a given parameter as function of the year) but with different letters vary significantly (P < 0.05).
species studied to the neighboring plant species
and conversely.
Concentration in total sugar of the nectar of
plant species studied
Results from Table 7 reported the mean
concentration in total sugar of B. steppia nectar
was 38.07% (n = 62; s = 9.60) in 2017 and
36.29% (n = 45; s = 9.69) in 2018. The difference
between these means is not significant (t = 0.94;
df = 105; P > 0.05). The mean concentration in
total sugar of the C. africana nectar was 19.43%
(n = 60; s = 3.42) in 2017 and 19.05% (n = 73; s =
3.25) in 2018. The difference between these two
means is not significant (t = 0.65; df = 131; P >
0.05). The mean concentration in total sugars of
P. viridiflorum nectar was 29.54% (n = 46; s =
6.63) in 2017 and 28.84% (n = 69; s = 6.14) in
2018. The difference between these means is not
significant (t = 0.58; df = 113; P > 0.05). The mean
concentration in total sugar of P. mahonii nectar
was 26.03% (n = 37; s = 1.03) in 2017 and
25.97% (n = 43; s = 0.96) in 2018. The difference
between these means is not significant (t = 0.26;
df = 78; P > 0.05). The difference was significant
between the four plant species concerning this
parameter in 2017 (F = 7.14; df = 3, 201; P <
0.05) and in 2018 (F =5.31; df = 3, 226; P < 0.05).
Overall, the concentration in total sugar of the
nectar varies following plant species.
Apicultural value of the plant species
During the flowering period of each plant species
studied, we recorded distinct levels of activity of A.
mellifera workers on the flowers. There were a
high availability of flowers, a high density of
workers per tree or shrub, a good nectar collection
on all plant species and high pollen harvest on B.
steppia but a low pollen collection on P.
viridiflorum. Moreover, in the dry season, which is
the main period of honey flow, individual tree of P.
viridiflorum and P. mahonii investigated could
produce more than 70.000 flowers. On the other
hand, during the rainy season (period of the food
shortage within honeybee colonies), individual
tree of B. steppia and C. africana could averagely
produce up to 15.000 flowers. Considering these
data, the plant species studied can be classified
based on their apicultural value as follows: (a)
very highly nectariferous: C. africana, and P.
mahonii; (b) very highly polliniferous and slightly
nectariferous: B. steppia (c) very highly
nectariferous and slightly polliniferous: P.
viridiflorum. Table 8 summarizes the appropriate
period for the optimal nectar and/or pollen
availability in Nyambaka in 2017 and 2018. Thus,
in this study area, the nutritional requirements of
honeybees are provided by B. steppia from
August to September, C. africana from June to
August while P. viridiflorum and P. mahonii were
important suppliers of nectar to foragers from April
to May.
Impact of A. mellifera activity
pollination of the plant species
on
the
During the collection of pollen or nectar on the
flowers of the four plant species studied, foragers
regularly contacted anthers and carried pollen.
With this pollen, they flew frequently from flower to
flower. The percentage of the total number of
visits during which worker bees came into contact
with the stigma of the visited flower was 100% for
Mbere et al.
1285
Table 8. Apicultural value of plant species studied and the most favorable period for bees to harvest nectar and/or pollen.
Floral product harvested
Nectar
Pollen
**
****
****
****
**
****
-
Plant species
Bidens steppia
Cordia africana
Pittosporum viridiflorum
Psychotria mahonii
Intense blooming period
September-October
July-August
April-May
April-May
**** = very high nectariferous or polliniferous; ** = slightly nectariferous or polliniferous.
Table 9. Number and frequency of contacts between Apis mellifera and the stigma during the floral visits to three plant species.
March-November 2017
Plant species
Bidens steppia
Cordia africana
Pittosporum viridiflorum
Psychotria mahonii
Number of studied visits
450
253
331
552
March-November 2018
Visits with stigmatic
contact
Number
450
253
331
552
%
100.00
100.00
100.00
100.00
Number of
studied visits
692
306
343
172
Total
Visits with stigmatic
contact
Number
692
306
343
172
%
100.00
100.00
100.00
100.00
Number of visits
studied
1142
559
674
724
Visits with
stigmatic
contact
Number
%
1142
100.00
559
100.00
674
100.00
724
100.00
Number and frequency of contacts comparison: (Bidens steppia) : χ2 2017/2018 = 0.00 ; df = 1; P > 0.05 ; (Cordia africana) : χ 2017/2018 = 0.00 ; df = 1 ; P > 0.05 ; (Pittosporum viridiflorum) : χ
NS
2
NS
2
NS
2017/2018 = 0.00 ; df = 1 ; P > 0.05 ; (Psychotria mahonii ) : χ 2017/2018 = 0.00 ; df = 1 ; P > 0.05 ; (B. steppia, C. africana, P. viridiflorum, Ps. mahonii) : χ 2017 = 0.00 ; df = 3; P > 0.05 ; (B.
2
NS
steppia, C. africana, P. viridiflorum, P. mahonii) : χ 2018 = 0.00; df = 3 ; P > 0.05 .
NS
B. steppia, C. africana P. viridiflorum and P.
mahonii during the 2017 as well as the 2018
investigation period (Table 9). Consequently, A.
mellifera workers strongly increase the pollination
possibilities of B. steppia, C. africana, P.
viridiflorum and P. mahonii.
DISCUSSION
In Nyambaka, an important area for beekeeping
2
practice in the Adamawa region of Cameroon, the
four plant species studied have shown their
importance as sources of pollen and nectar for
African honeybees. Previous works have already
been done in other countries which have shown
the immense potential that some of these plant
species abounded in the local beekeeping
practice. That is the case for C. africana which
was mentioned in the Western Amhara region of
Ethiopia as a major honeybee plant (Tesfa et al.,
2013); moreover, the pollen of this plant species
NS
2
was identified as the secondary pollen source in
four honey samples collected from Salika village
in Ethiopia (Tewelde, 2006). The collection of the
nectar of P. psychotroides by A. mellifera, another
plant species belonging to the genus Psychotria,
has already been reported in previous
investigations in the Adamawa Region (Dongock
et al., 2017). In Benin, Yédomonhan et al. (2009)
found that, on the flowers of Psychotria spp., A.
mellifera harvested both pollen and nectar widely.
In the southern highland of Tanzania, the flowers
1286
Afr. J. Agric. Res.
of B. steppia and P. viridiflorum were mentioned as an
important source for both pollen and nectar collection all
day long and during the whole flowering period (Latham,
2015). In Bujumbura (Burundi), B. steppia flowers were
mainly visited by the honeybee (Ndayikeza et al., 2014)
for both nectar and pollen collection. Overall, the
substance harvested by A. mellifera from flowers (nectar
or pollen) on a given plant species can vary with regions.
The variations observed in this study could be explained
mainly by the real needs of the colonies from which
originated honeybee workers (Segeren et al., 1996). The
good nectar collection observed in the four plant species
is the fact that, bees can collect nectar with sugar
concentrations below 15-85% under natural conditions
(Roubik and Buchmann, 1984).
From our fieldwork, the colors of the flowers of the
studied plant species are among the most attractive for
honeybee foragers. According to Bergström (1982), the
bright colors are the most attractive for the flower-visiting
insects in general and honeybees in particular because
those are among the colors they can easily perceive.
Indeed, bees have a much broader range of color vision.
Their ability to see ultraviolet light gives them an
advantage when seeking nectar and pollen (Dyer and
Garcia, 2014). Thus, to identify the most profitable
flowers, and avoid non-rewarding flowers like mimics
(Dafni, 1984), bees make use of several cues including
color (Hempel et al., 2001) information. Furthermore,
several other parameters such as the accessibility of
nectar and/or pollen, the availability of both products, the
floral mass or number of flowers or inflorescences
bearded by a plant species are important for the good
practice of beekeeping elsewhere (Segeren et al., 1996).
Another important aspect from the present study is the
possibility of the mastery of the period when the
blossoming of each plant species studied is effective and
optimal yearly. Indeed, the knowledge of these time
intervals makes it possible to establish the apicultural
calendar in avoiding pollen and nectar scarcity and
shortage (Chigere et al., 2014). For this purpose, the
supply of A. mellifera foragers with nectar and/or pollen in
a well-known period of the year is already possible for B.
steppia, C. africana, P. viridiflorum and P. mahonii in the
study site.
The observed high abundance of foragers per 1000
flowers recorded in this study could be attributed to the
ability of honeybees to recruit a great number of workers
for the exploitation of high-yield food sources (Frisch,
1969; Kajobe, 2006). Honeybees can smell or detect
pollen or nectar odor (Free, 1970) using sensory
receptors located on the flagellum of their antennae.
Worker honeybees dance inside the nest after a
successful foraging trip to communicate with their
congeners, information about the food odor, the distance
and the direction from the hive to the food source (Frisch,
1967). The round dance is performed when the resource
is within 100 meters from the hive, while the wagging
dance takes place for the resource 100 meters away from
the hive (Frisch, 1967).
Significant differences observed between the duration
of pollen harvesting visit and that of nectar harvesting on
the flowers of B. steppia could be explained by the
accessibility of each of these floral products. On the
flower of B. steppia, pollen is a product in great quantity
and is easily accessible to bees. In these conditions,
honey bee workers can obtain their pollen load by visiting
a few flowers during a foraging trip. That is why A.
mellifera spent more time on a flower for pollen
harvesting than for nectar in B. steppia. Therefore, on
each of the four plant species, A. mellifera spent more
time on a flower for nectar collection of C. africana, B.
steppia, P. mahonii and P. viridiflorum respectively. The
fact that A. mellifera spent significantly different time on a
flower of different species for nectar and pollen collection
could be explained by the abundance and/or the
accessibility to each of these floral products.
The disruptions of visits by other insects reduced the
duration of certain A. mellifera visits. This obliged some
workers to visit more flowers during a foraging trip, to
maximize their pollen or nectar loads. Similar
observations were made for A. mellifera workers foraging
on flowers of Entada africana (Fabaceae), Eucalyptus
camaldulensis (Myrtaceae), Psidium guajava (Myrtaceae)
and Trichillia emetica (Meliaceae) (Tchuenguem et al.,
2007), Combretum nigricans (Combretaceae), Erythrina
sigmoidea
(Fabaceae),
Lannea
kerstingii
(Anacardiaceae), Vernonia amygdalina (Asteraceae)
(Tchuenguem
et
al., 2010),
Jatropha
curcas
(Euphorbiaceae), Senegalia polyacantha (Mimosaceae)
and Terminalia schimperiana (Combretaceae) (Wékéré et
al., 2018)
The present study shows that during one foraging trip,
an individual bee foraging on a given plant species
scarcely visited another plant species. This result
indicates that A. mellifera shows flower constancy
(Louveaux, 1984) for the flowers of each of the four plant
species studied. This floral constancy in honeybees
exists because an individual forager is generally capable
of memorizing and recognizing the shape, color, and odor
of the flowers visited during previous foraging trips (Hill et
al., 1997; Wright et al., 2002). The flower constancy of A.
mellifera has been demonstrated on flowers of several
other plant species among which are Jatropha curcas
(Euphorbiaceae), Senegalia polyacantha (Mimosaceae)
and Terminalia schimperiana (Combretaceae) (Wékéré et
al., 2018), Lannea kerstingii (Anacardiaceae) and
Ximenia americana. (Olacaceae) (Djonwangwé et al.,
2011), and Callistemon rigidus (Myrtaceae) (Fameni et
al., 2012). The faithfulness of the honeybee to the flowers
of the plant species studied can also be explained, in
part, by the fact that their nectar is rich in sugars; Philippe
(1991) suggested that foragers could not allow their
colony to record a net energy gain if the sugar
concentration of the harvested nectar is less than 20%.
Mbere et al.
Considering this minimum limit, browsers can allow their
colony to gain a lot of energy when they collect nectar
from plant species studied.
During the collection of nectar and/or pollen on each
flower, A. mellifera workers regularly come into contact
with the stigma and anthers. They could thus enhance
self-pollination, which has been demonstrated for other
plant species in the past (Anderson and Symon, 1988;
Lewis et al., 1999; Otiobo et al., 2015). A. mellifera could
induce cross-pollination through carrying of pollen with
their furs, legs and mouth accessories, which is
subsequently deposited on another flower belonging to
different plants of the same species (Abrol, 2012).
Conclusion
At Nyambaka, A. mellifera workers harvested intensely
and regularly the nectar and pollen of B. steppia, C.
africana, P. viridiflorum and P. mahonii flowers. These
results suggest that these plants are the highly
nectariferous and polliniferous floral plant able to
substantially contribute to maintaining the nutritional
needs of the honeybee colony. All these plant species
contributed more or less to the feeding and therefore to
the strengthening of the honeybee colonies. A. mellifera
workers increased the pollination possibilities of each
plant species. Based on our results, we recommend: (a)
the installation of A. mellifera colonies in environments
where one or more of the studied plant species occur
abundantly and (b) the plantation and/or protection of
each plant species in the surrounding of A. mellifera
apiaries. These precautions will allow, in addition to
improving the production of honey in the study location,
its enrichment in various therapeutic properties for the
well-being of the local populations. The impact of A.
mellifera on fruit or grain yields of each plant species
studied via its pollination efficiency will be looked at in
future works.
CONFLICT OF INTERESTS
The authors have not declared any conflict of interests.
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