Foraging Behaviour of the African Honey Bee (Apis
mellifera adansonii) on Annona senegalensis, Croton macrostachyus, Psorospermum febrifugum and Syzygium guineense var. guineense
Flowers at Ngaoundere (Cameroon)
Fernand-Nestor Tchuenguem Fohouo,
To determine the apicultural value of Annona senegalensis
Pers. 1806 (Annonaceae), Croton macrostachyus Hochst. Ex Del. 1847
(Euphorbiaceae), Psorospermum febrifugum Spach 1836 (Hypericaceae)
and Syzygium guineense (Will.) DC var. guineense 1828 (Myrtaceae),
Apis mellifera adansonii Latreille 1804 (Hymenoptera: Apidae) activity
was observed on their flowers in the area of Ngaoundere, from January
to May, in 2002 and 2003. Flowers of each plant species were prospected
at least four days per month, between 7 am and 6 pm, for the registration
of the nectar and/or pollen foraging behaviour of A. m. adansonii
workers. Results show that A. m. adansonii harvested nectar and
pollen of each plant species. The greatest number of workers foraging
simultaneously on a plant varied from 9 in P. febrifugum to 3600
in S. g. guineense. A. m. adansonii workers were faithful
to each plant species. A. senegalensis, C. macrostachyus, P. febrifugum and S. g. guineense could be cultivated and
protected to increase honey production. A. senegalensis could enable
beekeepers to increase their pollen production as a hive product. During
foraging, A. m. adansonii workers increased pollination possibilities
of each plant species.
to cite this article:
Fernand-Nestor Tchuenguem Fohouo, Denis Djonwangwe and Dorothea Bruckner, 2008. Foraging Behaviour of the African Honey Bee (Apis
mellifera adansonii) on Annona senegalensis, Croton macrostachyus, Psorospermum febrifugum and Syzygium guineense var. guineense
Flowers at Ngaoundere (Cameroon). Pakistan Journal of Biological Sciences, 11: 719-725.
The basic foods of each honey bee colony are nectar and
pollen (Crane, 1999; Weidenmuller and Tautz, 2002). Nectar is transformed
into honey. Pollen and honey are stored in the hive for future use. These
substances have been exploited by human for million of years (Crane, 1999).
Honey and pollen production depends mainly on the abundance of some plant
species and their attractiveness to honey bees (Williams and Carreck,
1994; Segeren et al., 1996). Thus the sustainable beekeeping in
a given region needs a detailed knowledge of the bee plants which grow
in the environment of the hives (Segeren et al., 1996; Riedacker, 1996;
Bakenga et al., 2000).
Before this study, literature is scant on the relationships
between the honey bee and many plant species in Cameroon. Nevertheless,
in this country, owing to increasing demand for hive products such as
honey and pollen, beekeeping needs to be developed. Highest quantities
of honey consumed or marketed in Cameroon came from the Adamawa region
which has a climate particularly favourable to the proliferation of bees
(Inades, 2000a). Despite this attribute, the region is equally concerned
by the problem of low beekeeping production (Inades, 2000b).
The main objective of this research undertaken in Ngaoundere
during the dry season and the beginning of the rainy season (period of
the highest honey production by honey bees in this region) of 2002 and
2003 was to contribute to the knowledge of the relationships between honey
bees and A. senegalensis, C. macrostachyus, P. febrifugum and
S. g. guineense. This knowledge is essential for an efficient management
of these plants.
For each plant species, specific objectives were, the registration
of the activity of A. m. adansonii on flowers, the estimation of
the apicultural value and the evaluation of the efficiency of A. m.
adansonii as pollinator.
MATERIALS AND METHODS
Site and biological materials: Studies took place from January
to May, in 2002 and 2003 at Dang, a village of Ngaoundere in the Adamawa
region. This region belongs to the high altitude guinean savannah agro-ecological
zone. The climate is characterized by two seasons: a rainy season (April-October)
and a dry season (November-March). The annual rain fall is about 1500
mm. The mean annual temperature is 22°C. The mean annual relative humidity
Plants chosen for observations were located on an area of
3 km in diameter, centred on a Kenyan top-bar hive inhabited by an A.
m. adansonii colony. The hive is located at the latitude 7°24.949`N,
the longitude 13°32.870`E and the altitude 1093 masl. The number of honey
bee colonies located in this area varied from 32 in December 2001 to 67
in January 2002. The vegetation was represented by crops, ornamental plants,
hedge plants and native plant species of the savannah and gallery forests.
Table 1 describes plant species studied.
For each of these plant species, Table 2 shows the relative
abundance of opened flowers per month, during the two studied periods.
Study of the foraging activity of A. m. adansonii on flowers:
From the 1st January 2002 to 31 May 2002, then from 1st January 2003
to 31 May 2003, at least 4 days per month (preferably on Sundays), between
7 am and 6 pm, period divided into three hourly brackets (7-11 h, 11-15
h and 15-18 h), flowers of different plant species were observed for the
registration of the foraging behaviour of A. m. adansonii workers.
Table 3 gives the number of observation days for each plant. For each
plant species which flowers are visited by these bees and for each observation
date, the following parameters were registered for each hourly bracket
and if possible, on at least 10 individual plants: floral product (nectar
or pollen) harvested during each floral visit, abundance of foragers (greatest
number of individuals foraging simultaneously on a flower or an individual
plant), duration of individual flower visit (using stopwatch), influence
of the fauna (disruption of foragers activity by competitors or predators)
and impact of the competitive flora (attractiveness of other plant species
with respect to A. m. adansonii). The influence of the competitive
flora was assessed by two methods: a) direct observation on the relationships
between honey bee workers foraging on a given plant species and other
plant species in flower near the plant under observation; b) study of
the pollen loads carried by A. m. adansonii workers caught on the
flowers of C. macrostachyus and S. g. guineense: during
each of the three days of full flowering, each day, two pollen foragers
have been caught on flowers of each of these two plant species; pollen
loads of each worker were then remove from pollen baskets and subjected
to the microscopic analysis for the determination of the pollen profile.
Evaluation of the apicultural value of different plant species: Like
for other plant species, (Guerriat, 1996; Tchuenguem Fohouo et al.,
2004), the apicultural value of each plant studied was evaluated using
data on the flowering intensity and the attractiveness of A. m. adansonii
workers with respect to nectar and pollen.
Evaluation of the influence of A. m. adansonii on pollination:
To measure the ability of A. m. adansonii to act as pollinator
of each plant species, visits during which the forager came into contact
with the stigma were counted together with the duration of the flower
visits (Freitas, 1997).
Data analysis: Data were analysed using descriptive statistics,
student`s t-test for the comparison of means of two samples, Correlation
coefficient (r) for the evaluation of the association between two variables
and Microsoft Excel.
||Scientific name, botanic
family, biotope, some characteristics and strength (in the observation
station) of different plants studied
|+: Spontaneous plant; tr: tree; sh:
shrub; FP: Flowering Period; DCOF: Dominant Colour of Opened Flower
||Relative abundance of opened flowers
according to plant species and time
1: <=100 flowers
= rare; 2: >100 and <=500 flowers = little abundant; 3: >500
and <=1000 flowers = abundant; 4: >1000 flowers = very abundant
m. adansonii foraging activity on flowers Floral
product harvested, intensity and frequency of collection of different
products The identity of the foods harvested by A. m. adansonii
workers on flowers of each plant species under investigation as well as
the intensity and the frequency of the collection of each food are shown
in Table 3 and 4.
The analysis of Table 3 reveals that: a)
on the flowers of each plant species, A. m. adansonii workers collect
nectar and pollen; b) the type of floral products foraged by A. m.
adansonii on a given plant species can vary with time; c) in general,
the intensity (very weak, weak, high, very higher) of nectar or pollen
collection vary with plant species and time; d) considering plant species
on which honey bees harvest nectar, frequency (percentage compare to the
number of observation days) of harvest of this food varies from 43.75%
in S. g. guineense to 100% in C. macrostachyus; e) for the
plant species on which honey bees harvest pollen, the harvesting frequency
(percentage compare to the number of observation days) varies from 18.75%
in P. febrifugum to 100% in C. macrostachyus and S. g.
The simultaneous analysis of Table 2 and
3 suggests that in general, the intensity of nectar or
pollen collection by honey bees coincides more or less with the flowering
rhythm of the corresponding plant species.
Table 4 shows that during the day time,
the type of flower substance harvested by A. m. adansonii on a
given plant species can varies with hourly brackets.
Density of foragers: The greatest number of A. m. adansonii
workers foraging simultaneously was 1 per flower of each of the studied
plant species. Table 5 shows that the abundance of A.
m. adansonii workers per individual plant varies from 9 (P. febrifugum
in March 2002 and 2003) to 3600 (S. g. guineense in February 2003).
Duration of visits per flower: Table 6 indicates
that in general: a) the mean duration of a flower visit varied with plant
species and for a plant species, with the type of floral product collected;
b) the mean duration of a visit per flower did not vary significantly
from year to year.
The difference between the mean duration of a flower visit
for nectar collection and that for pollen collection was highly significant
in A. senegalensis (2002: t = 12.25, p<0.001; 2003: t = 10.90,
p<0.001) and in S. g. guineense (2002: t = 6.68, p< 0.001; 2003:
t = 5.57, p<0.001). Thus in A. senegalensis A. m. adansonii
spent more time on a flower for pollen collection than for nectar. In
S. g. guineense this bee spent more time for nectar collection
than for pollen.
The duration of visits was partially influenced by the anthophilous
fauna via disruptions. Thus for 165 honey bee workers visits registered
on C. macrostachyus in 2002, 19 were disrupted by other A. m.
adansonii (12 visits), Paratrechina longicornis (Latreille
1802) (3), Camponotus flavomarginatus Mayr 1862 (3) and Belonogaster
juncea Fabricius 1781 (1). For 108 visits registered on S. g. var.
guineense flowers in 2003, 41 were disrupted by other A. m. adansonii
(21), Lasioglossum sp). (13), Xylocopa calens Lepeletier
1841 (3), Calliphora sp. (2) and B. juncea (2).
Influence of neighbouring flora: During the observation periods
of each of the plant species under investigations, flowers of many other
plant species growing in the study area were visited by A. m. adansonii
workers, for nectar or pollen.
During one foraging trip, an individual bee foraging on
a given plant species scarcely visited another plant species (for each
plant species studied, not more than three observations of such behaviour,
for the study period). In addition, the analysis of the pollen loads collected
from the pollen baskets of some worker bees shows that the percentage
of the foreign pollen grain varied from 0.56% in S. g. guineense
to 4.82% in C. macrostachyus (Table 7).
by A. m. adansonii on flowers of various plant species
according to time, harvesting intensity and frequency of each
P: Pollen; 1, 2, 3, 4 in superscript, respectively: very low,
low, high, very high collections; TD: Total number of observation
days; nDN: Number of days where collection of nectar was observed;
pDN: percent of days where collection of nectar was observed;
nDP: Number of days where collection of pollen was observed;
pDP: Percent of days where collection of pollen was observed
by A. m. adansonii on flowers of various plant species
according to hourly brackets, following the 2002-2003 investigation
A. m. adansonii workers per plant (maximum of individuals
simultaneously in activity on opened flowers for three observations)
according to plant species and months
||Visiting time of A. m. adansonii
on flowers of different plant species according to the study periods
and harvested products
n: Number of
visits studied, m: Mean; s: Estimated standard deviation; min:
minimum; max: maximum; N: Nectar collection visits; P: Pollen
collection visits; NS: Non significant difference
of pollen loads collected in the corbiculae of some A. m.
adansonii workers foraging on flowers of two plant species
according to the investigation periods
americana L. 1753 (Olacaceae); Ea: Entada africana
Guill. and Perr. 1832 (Mimosaceae); Ec: Eucalyptus camaldulensis
Dehnh. 1832 (Myrtaceae)
Apicultural value of the plant species: During the observation
period, we noted a well elaborated activity of A. m. adansonii
workers on the flowers of each plant species. In particular, there were
high density of workers per tree, good nectar collection on A. senagalensis,
C. macrostachyus and S. g. guineense, high pollen collection
on A. senegalensis, weak nectar collection on P. febrifugum,
weak pollen collection on C. macrostachyus, S. g. guineense and
P. febrifugum (Table 3) and constancy on flowers
of each plant species. Furthermore, our field observations revealed that
in the dry season (main period of honey flow), individual tree of each
plant species under investigation could produce more than 20000 flowers.
These data allow plant species studied to be classify in
four categories of bee plants: a) highly nectariferous: C. macrostachyus,
S. g. var. guineense and A. senagalensis; b) slightly nectariferous:
P. febrifugum; c) highly polliniferous: A. senegalensis;
d) slightly polliniferous: C. macrostachyus, P. febrifugum and
S. g. guineense (Table 8).
Table 8 shows the appropriate period to harvest honey or
pollen in hives installed in an area of at least 3 km in diameter where
flora in bloom is mainly made up of a strong population of each of the
plant species with high apicultural value according to the investigation
of the period 2001-2003. Considering the study region, it emerges from
this table that in the Adamawa region of Cameroon: a) honey can be harvested
in March, May and June, if the environment of apiary is dominated by a
strong population of S. g. guineense, A. senegalensis and C.
macrostachyus, respectively; b) pollen can be
value of various plant species and the most indicated period
to harvest honey and /or pollen from hives installed in environment
where the flowering vegetation is predominantly characterised
by a high population of corresponding plant species in a delimited
area of at least 3 km in diameter, following the 2002-2003 investigation
2 = Low nectariferous value; 3: High nectariferous value; 4
= Very high nectariferous value, 3rd column: 1 = Very low polliniferous
value; 2 = Low polliniferous value; 3 = High polliniferous value
||Number and frequency of contacts
between A. m. adansonii and the stigma during the floral
visits of two plant species
harvested in the hives in April, if the environment of the
apiary is dominated by a strong population of A. senegalensis.
Impact of A. m. adansonii activity on pollination of the plant
species: During the collection of pollen or nectar on flowers of each
plant species, 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 varied from 83.49% in S. g. guineense
to 100% in A. senegalensis (Table 9).
The collection of nectar and pollen of C. macrostachyus
by A. m. adansonii has also been noted in Ethiopia (Fichtl and
Adi, 1994). In West Cameroon, A. m. adansonii collects only the
nectar of this Euphorbiaceae (Dongock Nguemo et al., 2004). The
collection of the nectar of S. g. guineense by A. m. adansonii
has also been observed in Ethiopia (Fichtl and Adi, 1994). Thus the type
of floral products harvested by A. m. adansonii on a given plant
species can vary with the regions and years. The observed variations could
be mainly explained by the availability of pollen or nectar at the level
of flowers and by the needs of the colonies of the foraging bees.
The observed high densities of foragers per tree were due
to the ability of honey bees to recruit a great number of workers for
the exploitation of high yield food sources (Frisch, 1969; Louveaux, 1984;
Schneider and Hall, 1997).
In A. senegalensis the fact that A. m. adansonii
spent more time on a flower for pollen harvest than for nectar could be
explained by the abundance and/or the accessibility to each of these floral
products: in this plant species, pollen is produced in great quantity
and is easily accessible to bees; in contrast, nectar is produced in small
quantity and is less accessible to bees. Under these conditions, a worker
honey bee can obtain its pollen load by visiting a few flowers during
a foraging trip.
In S. g. guineense, the fact that A. m. adansonii
spent more time on a flower for nectar collection than for pollen collection
could be explained by the abundance of each of these floral products:
in this plant species, pollen is produced in small quantity by anthers,
which are situated on the top of stamen and are thus easily accessible
to bees, whereas nectar is produce in great quantity between the base
of style and the stamens and is thus less accessible. Under these conditions,
a worker honey bee can obtain its nectar load by visiting few flowers
during a foraging trip. Similar results were found in Callistemon rigidus
R. Br. 1819 (Myrtaceae) (Tchuenguem Fohouo et al., 1997, 2004).
The disruptions of visits reduced the duration of certain
A. m. adansonii visits. This obliged some worker bees to visit
more flowers during a foraging trip, in view to obtain their maximal pollen
or nectar loads.
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. m. adansonii shows flower constancy
(Louveaux, 1984; Basualdo et al., 2000) for the flowers of each
plant species studied. This floral constancy is due to the fact that in
honey bees, individual forager is generally capable of memorizing and
recognizing the shape, colour and odour of the flowers visited during
previous foraging strips (Hill et al., 1997; Wright et al.,
Since C. macrostachyus, S. g. guineense and A.
senagalensis are highly nectariferous bee plants, they should be planted
and protected to increase honey production. Besides, C. macrostachyus
pollen has been identified in the honey collected in the study area in
2001 (3 samples of the 3 samples analysed) (Tchuenguem Fohouo, 2005).
S. guineense pollen has been identified in honey samples collected
in the same study area in 1999 and 2000 (7 samples of the 7 samples analysed)
(Mbofung et al., 2000), then in 2001 and 2002 (11 samples of the
11 samples analysed) (Tchuenguem Fohouo, 2005).
As a highly polliniferous bee plant, A. senegalensis
could permit the increase of pollen production as a hive product.
All the plant species studied contributed more or less to
the feeding and thus to strengthen honey bee colonies. Consequently, they
should be planted and protected in the environment of the apiaries.
We have seen that, during the collection of pollen or nectar
on flowers of each plant species, A. m. adansonii foragers regularly
contacted anthers and carried pollen with which they flew frequently from
flower to flower. Thus A. m. adansonii workers could induce self
pollination, by applying the pollen of a flower on the stigma of the same
flower. Foragers carried pollen from a flower of one tree to the stigma
of another flower of the same tree (geitonogamy) or to that of another
tree (xenogamy). Consequently A. m. adansonii workers increase
the pollination possibilities of C. macrostachyus, S. g. guineense,
A. senagalensis and P. febrifugum flowers.
Installation of A. m. adansonii colonies near the
population of each plant species studied should be recommended. Furthermore,
insecticide treatments should be avoided during the flowering period of
each plant species studied. If these treatments are necessary, the choice
of the insecticides that are less toxic for bees or the integrated pest
control should be recommended to protect pollinating insects such as A.
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