# Study on the foraging and pollinating activities of *Apis mellifera* L., 1758 (Hymenoptera: Apidae) on *Solanum aethiopicum* L., 1763 (Solanaceae) in Dang (Ngaoundéré, Adamawa, Cameroon)

Hassana Boubakari*(1), Azo'o Ela Michelson(1), Djonwangwé Denis(2) & Tchuenguem Fohouo Fernand-Nestor(3)

Des observations ont été faites à Dang (Adamaoua, Cameroun) sur les fleurs de *Solanum aethiopicum* au cours des saisons 2020 et 2021 pour évaluer l'influence des activités de butinage et de pollinisation d'*Apis mellifera* sur la production. Quatre traitements de 120 fleurs chacun ont été établis selon la protection (T₂ et T₆) ou non (T₁ et T₅) des fleurs contre les visites d'insectes, et l'ouverture puis la refermeture des fleurs après avoir reçu une visite d'A. mellifera (T₃ et T₇) ou sans visite d'insectes et de tout autre organisme (T₄ et T₈). Les visites florales d'A. mellifera ont été étudiées et les paramètres agronomiques évalués et comparés entre les traitements. *Apis mellifera* est apparu comme le principal insecte visiteur et pollinisateur de *S. aethiopicum* au cours des deux années d'investigation, avec une abondance relative moyenne de 41,07%. Cette espèce d'abeille récoltait exclusivement les grains de pollen sur les fleurs de *S. aethiopicum*. Son activité journalière débutait à 6 h avec l'épanouissement des fleurs et se terminait à 15 h avec leur fanaison ; un pic de visites florales a été noté entre 8 h et 9 h. La densité moyenne des abeilles était d'environ 340 individus/1000 fleurs et la vitesse de butinage variait de 4,1 à 6,77 fleurs/minute. Grâce à son efficacité pollinisatrice, A. mellifera a augmenté le taux de fructification, le taux moyen de graines par fruit et le taux de graines normales de *S. aethiopicum* de 15,46 %, 6,84 % et 7,60 % respectivement. La protection d'A. mellifera est essentielle pour l'amélioration des rendements au champ de *S. aethiopicum*.

**Mots-clés** : *Apis mellifera*, *Solanum aethiopicum*, pollinisation, rendement, Dang.

Observations were made in Dang (Adamawa, Cameroon) on *Solanum aethiopicum* flowers during the 2020 and 2021 seasons for assessing the influence of *Apis mellifera* foraging and pollination activities on yields. Four treatments of 120 flowers each were established according to the protection (T₂ and T₆) or not (T₁ and T₅) of the flowers from insect visits and isolating, opening, and reclosure of flowers after receiving a visit from A. mellifera (T₃ and T₇) or no insect visitors or other organisms (T₄ and T₈). Floral visits by A. mellifera were studied and the agronomic parameters were evaluated and compared between treatments. With a relative abundance of 41.07%, this bee species harvested exclusively pollen grains on *S. aethiopicum* flowers. The daily

<footnote>(1) Department of Biological Sciences, Faculty of Science, University of Maroua, P.O. Box 814, Maroua, Cameroon.</footnote>

<footnote>(2) Department of Life and Earth Sciences, Higher Teachers' Training College, University of Maroua, P.O. Box 55 Maroua, Cameroon.</footnote>

<footnote>(3) Department of Biological Sciences, Faculty of Science, University of Ngaoundéré, P.O. Box 454, Ngaoundéré, Cameroon.</footnote>

<footnote>* E-mail: hassabiyou@gmail.com</footnote>
activity of workers occurred between 6 a.m. and 3 p.m., with a peak of floral visits at 8 - 9 a.m. time interval. The mean density of bees was about 340 individuals/1000 flowers and the foraging speed varied from 4.1 to 6.77 flowers/minute. Through its pollination efficiency, *A. mellifera* increased the fruiting rate, the average rate of seeds per fruit, and the rate of normal seeds of *S. aethiopicum* by 15.46%, 6.84%, and 7.60% respectively. Protection of *A. mellifera* is essential for the improvement of *S. aethiopicum* field yields.

**Keywords:** *Apis mellifera*, *Solanum aethiopicum*, pollination, yield, Dang.

INTRODUCTION

Insects are key factors in food security in the world and essential links in the food chains (Nicolas *et al.*, 2013). Among these invertebrates, bees in general and singularly honeybees *Apis mellifera* Linnaeus, 1758 are the most important visitors and efficient vectors of pollen grains on plant species from flower to flower (Rosa *et al.*, 2010). *Apis mellifera* is therefore the major pollinator of several crops and wild plant species (Ollerton *et al.*, 2011). By visiting the flowers in searching for proteins and carbohydrates, workers facilitate the host plant breeding through its pollination activities (Klein *et al.*, 2007). Several previous findings are illustrative of the prominence of honeybees as the pollinator of wild plant species and crops: *Malus domestica* Stark Brothers, 1916 (Jacob-Remacle, 1989), *Cucumis sativus* Linnaeus, 1753 (Stanghellini *et al.*, 1998a,b, Gingrich *et al.*, 1999), *Anacardium occidentale* Linnaeus, 1753 (Freitas *et al.*, 2002), *Citrullus lanatus* (Thunberg) Mansf, 1916 (Kremen *et al.*, 2004; Azo'o *et al.*, 2017), *Helianthus annuus* Linnaeus, 1753 (Greenleaf and Kremen, 2006; Tchuenguem *et al.*, 2009a,b), *Ximenia americana* Linnaeus, 1927 and *Syzygium guineense* var. *guineense* Willd, 1828 (Djonwangwé *et al.*, 2011a,b), *Phaseolus coccineus* Linnaeus, 1753 (Pando *et al.*, 2011a,b), *Cucumeropsis mannii*, Naudin 1815 (Azo'o and Messi, 2012), *Callistemon rigidus* Robert Brown, 1857 (Fameni *et al.*, 2012), *Vigna unguiculata* (Linnaeus) Walpers, 1843 (Kengni *et al.*, 2015a,b), *Gossypium hirsutum* Linnaeus, 1763 (Basga *et al.*, 2019), or *Bidens steppia* Serff, 1923 (Mbere *et al.*, 2022). The pollination service of honeybees is an unvaluable contribution for maintaining biological balance in nature and enables animals, plants, and humans to thrive (Gallai *et al.*, 2009). Alongside the pollination activity on flowers, honeybees produce several products such as honey, propolis, wax, venom, and royal jelly (Tyburce, 1996). These products have multifunctional uses and are considered beneficial to health purposes (Molan, 2001).

One-third of human food and three-quarters of fruit, legume, oilseed, and protein crops depend on entomophilous pollination for their production (Terzo, 2007). African vegetables have been neglected for a long time and are now gradually being taken into account nationally and internationally (Seck, 2007). Cultivation of vegetables plays an important role in the income diversification strategies of urban and peri-urban populations (Kahane *et al.*, 2005). Growing them in home gardens is an effective way to improve the livelihoods of peasants in alleviating poverty (Betti *et al.*, 2016). Of the 275 most important vegetable species in tropical Africa, 207 are consumed for their leaves, approximately 37 for their fruits and over 31 species are used for their roots or tubers, especially their fruits such as the African eggplant *Solanum aethiopicum* (Kahane *et al.*, 2005).

Also called scarlet eggplant or Ethiopian eggplant, *S. aethiopicum* is a plant of the Solanaceae family (Silva *et al.*, 2004). It is mainly a fruit vegetable, but its hairless leaves are also eaten in southern Senegal and other African countries (Seck, 2007). Its edible fruits can be eaten at an advanced stage of ripening (Chen *et al.*, 2000). The fruits of *S. aethiopicum* are richer than those of tomato and European eggplant in calories, proteins, carbohydrates, and ash (Toury *et al.*, 1965).
The roots and fruits are used as carminative and sedative hypertensives, antiemetic and antidiarrheal (Agbankpe *et al.*, 2014). Leaf sap is also used as a sedative to treat uterine ailments (Jouzier, 2005; Diatta *et al.*, 2020).

The enhancement of crop yields using insects as a production factor still failed to appreciate in the rural sector by peasants in Cameroon (Tchuenguem et al., 2001). Yet, bees are nowadays recognized as indisputable agricultural inputs which allow a substantial increase in yields while preserving the integrity of the environment (Haubruge et al., 2007). Before our research, published data on the mutualism between S. aethiopicum and flower-visiting insects are from Nigeria (Oyelana and Ogunwenmo, 2012), Ivory Coast (Konan, 2013; Obodji et al., 2016; Felicia et al., 2019), and India (Latif et al., 2009). Apart from current studies, only works of Kengni et al. (2022) have been carried out on the foraging and pollination activity of an unidentified carpenter bee *Xylocopa* sp. on the Solanaceae in the Far-North region of Cameroon. The present study was defined to show the importance of honeybee activities in pollination and the production of African eggplant in the field study. Specific objectives were to i) determine the rank of honeybees *A. mellifera* in the floral entomofauna of the host plant; (ii) study the floral activity of bee workers on the flowers of the crop and, (iii) appreciate the consequence of the floral activity of *A. mellifera* on the pollination and yields of *S. aethiopicum*.

# MATERIALS AND METHODS

## Materials

Investigations were carried out from May to September 2020 and from May to August 2021 in Dang (Adamawa Region of Cameroon). This region belongs to the ecological zone with the high Guinean savannas (Djoufack-Manetsa, 2011). The climate in the Adamawa is of the Sudano-Guinean type, which has two seasons: a rainy season (April to October) and a dry season (November to March). The average annual temperature (°C) is 22±1 and the average annual humidity (%) is 70±16 (Ngaoundéré-airport meteorological station, 2022). The study site was an experimental field with 437 m² corresponding to the following geographical coordinates: latitude: 7°24'22.6"N, longitude: 13°32'52.3"E, altitude: 1085 m.

In addition to the insects naturally present in the environment of the study site, the animal material was enriched with an apiary of 36 and 42 colonies of *A. mellifera* in 2020 and 2021 respectively. The plant material consisted of *S. aethiopicum* seeds purchased in a store for the sale of agricultural equipment in Ngaoundéré. Technical equipment was used for setting up the experimental plot. Entomological equipment such as an entomological hand net, gauze bags, 70% diluted ethanol, and entomological boxes were used for capturing and preserving African eggplant flower-visiting insect specimens.

In Laboratory of Applied Zoology, University of Ngaoundéré, bee identifications were done by Prof. Tchuenguem Fohouo Fernand-Nestor, using reference collection and identification books (Delvare & Aberlenc, 1989; Borror & White, 1991; Eardley *et al*., 2010).

## Determination of the reproduction mode of African eggplant

At the appearance of the flower buds (August 29, 2020, and July 14, 2021), 240 of them were randomly selected on 15 stands per subplot for two treatments of 120 flowers each; a treatment X [T₁ (2020) or T₅ (2021)] with open-pollinated flowers and a treatment Y [T₂ (2020) or T₆ (2021)] where flowers were covered using 1 mm² mesh gauze bags (Figure 1). At maturity, the number of ripe fruits was counted, and the fruiting index (Ifr) was calculated in both treatments using the following formula: Ifr = Fb / Fa, where Fb is the number of fruits formed and Fa is the number
of flowers initially labeled (Tchuenguem *et al.*, 2001). The difference in fruiting indexes between treatments enables estimating the rate of allogamy (*TC*) and autogamy (*TA*) using both equations of Demarly (1977): $TC = \{[(IfrX - IfrY) / IfrX] * 100\}$, where IfrX and IfrY are the fruiting indexes in treatments X and Y respectively and the deduced $TA = (100 - TC)$.

<figure><img src="image_1.png" /><figcaption>**Figure 1:** *Solanum aethiopicum* plant showing unprotected flower (A), and protected with gauze bag (B).</figcaption></figure>

## Ranking of honeybees in the floral entomofauna of eggplant

During the flowering period of African eggplant, from August 29 to September 15, 2020 and from July 14 to August 29, 2021, observations were made every day on the flowers of treatments T₁ and T₃, following six daily time intervals: 6 - 7 a.m., 8 - 9 a.m., 10 - 11 a.m., 12 - 1 p.m., 2 - 3 p.m., and 4 - 5 p.m. The different flower-visitor species found were counted using the direct method and the cumulative results of counts were expressed as the number of visits (Tchuenguem *et al.*, 1997). Data on the frequency of forager visits enabled us to determine the rank of each one of them in the floral entomofauna of *S. aethiopicum*. The frequency of visits of a given insect *i* to the flowers of *S. aethiopicum* (*Fi*) was evaluated using the following equation: $Fi = [(Vi / Vt) * 100]$, where *Vi* is the number of visits of the insect *i* on the flowers from treatments X and *Vt* the number of visits of all the insects recorded (Tchuenguem *et al.*, 1997).

## Activity of Honeybees on the flowers of African eggplant

The proportion of collecting floral products (pollen or nectar) by *A. mellifera* on *S. aethiopicum* was noted when recording the length of visit per flower (Tchuenguem *et al.*, 2010). The nectar-sicker plunged its proboscis towards the nectaries while pollen collectors scraped the anthers using its mandibles and legs. The rhythm of honeybee activity according to the rhythm of eggplant blossoming daily was highlighted; moreover, the variation of the daily activity of foragers as a function of the time intervals was assessed. The duration of the floral products harvested was timed at the same dates as the frequency of visits, during the daily time slots mentioned above. The stopwatch, reduced to zero, was started as soon as a forager landed on a flower and stopped as soon as its lefts it. The duration of an individual visit corresponds to the value read on the stopwatch. The greatest number of individuals simultaneously active on a flower was recorded following direct counts. The abundance of foragers per 1000 flowers (*A*₁₀₀₀) was inferred using the following equation: $A_{1000} = [(Ax / Fx) * 1000]$, where Fx and Ax are respectively the numbers of blooming flowers and the number of foragers counted on opened flowers at time x (Tchuenguem *et al.*, 2004).
The foraging speed (Vb) or the number of flowers visited per minute was also recorded (Jacob-Remacle, 1989); the chronometer reduced to zero was triggered as soon as a forager landed on a flower and was stopped as soon as it was lost sight of; the number of flowers visited was counted during the foraging trip. Vb = [(Fi / di) * 60], where di is the duration given by the stopwatch (in seconds) and Fi is the number of flowers corresponding to di (Jacob-Remacle, 1989).

The foraging ecology which was considered consisted of the study of the abiotic factors influences such as temperature and relative humidity on the daily foraging rhythm of *A. mellifera*. During each day of observation, the temperature and relative humidity of the study station were recorded twice per observation time slot using a thermo-hygrometer. In addition, disruption of the activity of foragers by competitors or predators and the attractiveness exerted by other plant species on *A. mellifera* was assessed by direct observations (Tchuenguem, 2005). For the second parameter, the number of times that the bee left the Solanaceae flowers to another plant species and vice versa was noted through the investigation period (Tchuenguem, 2005).

## Repercussion of the foragers on production of African eggplant

In parallel with the implementation of treatments X and Y, 240 flower buds were labeled to constitute two other treatments consisting of 120 flowers each: a treatment A [T₃ (2020) or T₇ (2021)] whose flowers were intended for the pollinating efficiency of *A. mellifera* workers. As soon as each flower bloomed, the gauze bag placed the day before was removed to favor a single visit from a worker after which the flower was covered again; a Z treatment [T₄ (2020) or T₈ (2021)] whose initially protected flowers were opened and then reclosed without any visiting insect (Tchuenguem *et al.*, 2018).

At maturity, the fruits from treatments A and Z were harvested and compared. The assessment of the impact of flower-visiting insects on the fruit and seed production of *S. aethiopicum* was based on the estimates and comparisons of the fruiting rate, the average number of seeds, and the percentage of normal seeds per fruit between treatments X, Y, and Z. For a given treatment, the fruiting rate results from the ratio between the number of fruits formed and the number of flowers considered. The contribution of insect floral activity on the fruiting rate (*Fri*) was deduced using the equation: $Fri = {[(FX - FZ) / (FX + FY - FZ)] * 100}$, where FX, FY, and FZ are the fruiting rates in treatments X, Y and Z (Diguir *et al.*, 2020). Using the same method as for fruiting rate, the percentage of normal seeds due to flowering insects was deduced.

The contributions of *A. mellifera* to the fruiting rate, the mean number of seeds per fruit, and the percentage of normal seeds were also evaluated. The fruiting rate due to *A. mellifera* (*Fra*) was calculated using the following formula: $Fra = {[(FA - FZ) / FA] * 100}$ (Djakbé *et al.*, 2017). The percentage of normal seeds due to the pollinating action of honeybees was estimated using the same reasoning.

## Data analysis

Data were compiled in Excel 2013 and analyzed through descriptive statistics. The following statistic tests were hereby used: (i) the t-test of Student for comparing means between two samples, (ii) the Chi-square test ($\chi^2$) for the comparison of proportions between two samples, and (iii) the Pearson correlation coefficient (r) for establishing linear relationships between two data series from two equal size samples. The actual analyzes were facilitated using the software R 2.13.0.
# RESULTS

## Reproduction mode of *Solanum aethiopicum*

Fruiting indexes were 0.97, 0.86, 0.98 and 0.88 in treatments T₁, T₂, T₅ and T₆ respectively. The deduced *TC* and *TA* using these indexes were *TC* = 11.34% and *TA* = 88.66% in 2020 and *TC* = 10.20% and *TA* = 89.80%. The cumulative results from both years were *TC* = 10.77% and *TA* = 88.93%. Overall, *S. aethiopicum* shows a mixed reproduction mode with the prominence of autogamy on allogamy.

## Rank of *Apis mellifera* in the floral entomofauna of *Solanum aethiopicum*

In 2020 and 2021, 565 and 522 visits of 5 and 7 insect species were registered on 120 flowers of *S. aethiopicum*. Results from **table 1** are illustrative of insect species recorded and their relative abundance yearly. In both years, *A. mellifera* was the first flower visitor of *S. aethiopicum* with 41.07% of the frequency of visits. There is no significant difference between both proportions year to year ($\chi^2 = 0.67; df = 1; p > 0,001$).

<table><caption>**Table 1:** Flower-visitors of *Solanum aethiopicum* and their frequencies in 2020 and 2021.</caption><thead><tr><th rowspan="2">Order</th><th rowspan="2">Family</th><th rowspan="2">Genus and Species</th><th colspan="2">2020</th><th colspan="2">2021</th><th colspan="2">Total</th></tr><tr><th>n1</th><th>P1 (%)</th><th>n2</th><th>P2 (%)</th><th>Nt</th><th>Pt (%)</th></tr></thead><tbody><tr><td rowspan="5">Hymenoptera</td><td rowspan="4">Apidae</td><td><i>Apis mellifera</i></td><td>239</td><td>42.30</td><td>208</td><td>39.85</td><td>447</td><td>41.07</td></tr><tr><td><i>Amegilla</i> sp. 1</td><td>131</td><td>23.18</td><td>107</td><td>20.50</td><td>238</td><td>21.84</td></tr><tr><td><i>Amegilla</i> sp. 2</td><td>18</td><td>3.18</td><td>40</td><td>7.66</td><td>58</td><td>5.42</td></tr><tr><td><i>Xylocopa olivacea</i></td><td>-</td><td>-</td><td>15</td><td>2.87</td><td>15</td><td>1.43</td></tr><tr><td rowspan="3">Halictidae</td><td><i>Lasioglossum</i> sp. 1</td><td>100</td><td>17.69</td><td>73</td><td>13.98</td><td>173</td><td>15.83</td></tr><tr><td><i>Lasioglossum</i> sp. 2</td><td>77</td><td>13.62</td><td>69</td><td>13.22</td><td>146</td><td>13.42</td></tr><tr><td>Halictidea sp. 1</td><td>-</td><td>-</td><td>10</td><td>1.92</td><td>10</td><td>0.96</td></tr></tbody><tfoot><tr><td colspan="2">Total</td><td></td><td>565</td><td>100.00</td><td>522</td><td>100.00</td><td>1087</td><td>100.00</td></tr><tr><td colspan="2"></td><td></td><td colspan="2">5 species</td><td colspan="2">7 species</td><td colspan="2">7 species</td></tr></tfoot></table>

*n1*: number of visits in 2020; *n2*: number of visits in 2021; *Nt*: total sum of visits in 2020 and 2021; *P1*: percentages of visits in 2020; *P2*: percentages of visits in 2021; *Pt*: total sum of percentages of visits in 2020 and 2021; sp.: unidentified species; *P1* = (*n1*/565) * 100; *P2* = (*n2*/522) * 100.

## Floral products harvested

During their floral visits, workers of *A. mellifera* highly and exclusively collected pollen of *S. aethiopicum*. Indeed, the results recorded showed that among 200 visits studied for floral preference, the workers were only observed in the posture of collecting pollen (Figure 2).
<figure><img src="image_2.png" /><figcaption>**Figure 2:** Posture for pollen harvesting by *Apis mellifera* on an eggplant flower.</figcaption></figure>

## Rhythm of honeybee visits according to the daily rhythm of eggplant blossoming

Figure 3 shows the variation of the number of blooming flowers and the number of *A. mellifera* workers visits depending on the observation days. From this figure, the number of daily visits by *A. mellifera* was proportional to the number of daily opened flowers of *S. aethiopicum*. The correlation between both parameters was positive and significant in 2020 (r = 0.72; df = 4; p < 0.01) and in 2021 (r = 0.82; df = 4; p < 0.01). This result highlights the good attractiveness of the pollen of *S. aethiopicum* towards *A. mellifera*.

<figure><img src="image_3.png" /><figcaption>**Figure 3:** Seasonal variations of *Solanum aethiopicum* opened flowers and the honeybee worker visits.</figcaption></figure>

## Daily rhythm of worker visits as a function of time interval

Figure 4 shows the distribution of *A. mellifera* visits on the flowers of *S. aethiopicum* following the daily time slots defined. The floral activity of honeybees started at down 6 - 7 a.m. (flower anthesis) and stopped at 2 - 3 p.m. (flower wilting). An important peak of this daily activity occurred at the 8 - 9 a.m. time interval. There is a similarity in the daily rhythm of worker visits during both years.
<figure><img src="image_4.png" /><figcaption>**Figure 4:** Rhythm of floral activity of honeybees on eggplant following the daily time slots.</figcaption></figure>

**Density of workers**

The average density of workers per flower of *S. aethiopicum* was 1 (n = 54; s = 0) in 2020 and 2021 as well (n = 63; s = 0). The mean abundance per 1000 flowers were 337.03 (n = 54; s = 153.32) in 2020 and 317.46 flowers (n = 63; s = 155.06) in 2021. The difference of the two latter means between both years was not significant (t = 0.68; df = 115; p > 0.05) which is expressive of the stability of the field experiment yearly.

**Mean duration of a honeybee visits per flower.**

The mean length of a floral visit of *A. mellifera* varied from 35.16 sec (n = 100; s = 26.37) in 2020 to 35.03 sec (n = 113; s = 24.41) in 2021. The difference between both values was not significant (t = 0.04; df = 211; p > 0.05).

**Mean foraging speed**

On *S. aethiopicum*, a bee worker visited 1 to 51 flowers/min in 2020 then, 1 to 53 flowers/min in 2021 during a foraging trip. The mean foraging speed was 6.71 flowers/min (n = 111; s = 3.36) in 2020 and 4.10 flowers/min (n = 132; s = 2.59) in 2021. The difference was highly significant between both mean values (t = 6.77; df = 241; p < 0.001) and shows the variation of the foraging speed of workers from year to year.

**Influence of abiotic and biotic factors on the daily rhythm of activity of workers**

The correlations were not significant between the *A. mellifera* visits and the temperature in 2020 (r = 0.04; df = 4; p > 0.05) and in 2021 (r = 0.02; df = 4; p > 0.05), as well as between these visits and the relative humidity in 2020 (r = 0.35; df = 4; p > 0.05) and in 2021 (r = 0.61; df = 4; p > 0.05).

Workers of *A. mellifera* were disturbed in their foraging activity by other foragers of the same species or those from other species that were competitors for *S. aethiopicum* pollen. In 2020, for 100 visits of *A. mellifera*, 2 and 1 were interrupted by *A. mellifera* and *Amegilla* sp. 1 Friese, 1897 respectively. In 2021, for 113 visits, 3.53%, 1.76%, 0.88% and 0.88% were interrupted by *A. mellifera*, *Amegilla* sp. 1, *Lasioglossum* sp. 1 Curtis, 1833 and *Xylocopa olivacea* Fabricius, 1787 respectively.

During the flowering season of *S. aethiopicum*, flowers of many other plant species surrounding the field of this Solanaceae were visited by *A. mellifera*, for nectar (ne) or pollen (po). Among these plants were *Bidens pilosa* L., 1753 (Asteraceae, ne and po), *Hibiscus sabdarifa* L., 1753 (Malvaceae, ne) and *Zea mays* L., 1753 (Poaceae, po). During the two years of study, we observed no passage of *A. mellifera* from *S. aethiopicum* flowers to flowers of another plant species and vice
versa.

## Impact of flowering insect including *Apis mellifera* on the pollination and production of eggplant

During pollen harvesting, the worker constantly meets the reproductive organs of *S. aethiopicum* and moves from flower to flower with pollen grains adhered to its hair tegument. Therefore, honeybees were identified in this study as one of the active pollen transferors on *S. aethiopicum* flowers.

**Table 2** shows the fruit set rates, the mean number of seeds per fruit, and the percentage of normal seeds from flowers of *S. aethiopicum* according to treatments T₁ and T₂ in 2020 then T₅ and T₆ in 2021. Overall, the fruit set rate was higher in treatments with open-pollinated flowers (T₁ and T₅) than those whose flowers were covered for excluding insect foraging activity (T₂ and T₆). The difference of the fruit set rate was highly significant between T₁ and T₂ (χ² = 10.03; df = 1; *p* < 0.01) and between T₅ and T₆ (χ² = 9.64; df = 1; *p* < 0.01). The values of the fruit set rates due to the foraging activity of insects were 11.76% in 2020 and 17.32% in 2021, with a cumulative mean value of 14.54%.

<table><caption>**Table 2:** Production of eggplant according to treatments T₁, T₂, T₅ and T₆.</caption><thead><tr><th rowspan="2">Years</th><th rowspan="2">Treatments</th><th rowspan="2">NFS</th><th rowspan="2">NFF</th><th rowspan="2">FR</th><th colspan="2">NSF</th><th>TNS</th><th>NNS</th><th>% NS</th></tr><tr><th colspan="2">(%)</th><th colspan="2"></th></tr><tr><th></th><th></th><th colspan="8" style="text-align: center;">m</th><th colspan="2" style="text-align: center;">s</th></tr></thead><tbody><tr><td rowspan="2">2020</td><td>T₁</td><td>120</td><td>117</td><td>97.50</td><td>402.52</td><td>100.52</td><td>41041</td><td>39937</td><td>97.31</td><td></td><td></td></tr><tr><td>T₂</td><td>120</td><td>101</td><td>86.32</td><td>368.35</td><td>89.82</td><td>33668</td><td>30742</td><td>91.31</td><td></td><td></td></tr><tr><td rowspan="2">2021</td><td>T₅</td><td>120</td><td>118</td><td>98.33</td><td>391.79</td><td>131.42</td><td>43881</td><td>43053</td><td>98.11</td><td></td><td></td></tr><tr><td>T₆</td><td>120</td><td>106</td><td>88.33</td><td>330.29</td><td>123.39</td><td>32039</td><td>28895</td><td>90.19</td><td></td><td></td></tr></tbody></table>

NFS: number of flowers studied; NFF: number of fruits formed; FR: Fruiting rate; NSF: number of seeds/fruit; TNS: total number of seeds; NNS: number of normal seeds; %NS: percentage of normal seeds; T₁ and T₅: unprotected flowers; T₂ and T₆: protected flowers; m: mean; s: standard deviation.

From the same **table 2**, the mean number of seeds per fruit was higher in treatments T₁ and T₅ than in treatments T₂ and T₆. The difference between the mean value of seeds per fruit from both treatments was significant in 2020 (*t* = 2.54; *df* = 216; *p* < 0.05) and high significant in 2021 (*t* = 3.60; *df* = 222; *p* < 0.001). The deduced mean number of seeds per fruit of eggplant which resulted from the floral activity of its visitors was 7.06% in 2020 and 6.83% in 2021, with a cumulative mean value of 6.94%.

The percentage of normal seeds was less important in bagged clusters than on exposed-pollinated flowers of corresponding treatments. The insects' floral activity was responsible for the percentage improvement of normal seeds by 9.57% in 2020 and 5.35% in 2021, with a cumulative result of 7.46% for both experiments.
## Pollination efficiency of *Apis mellifera* on *Solanum aethiopicum*

**Table 3** shows the fruit set rate, the mean number of seeds per fruit, and the percentage of normal seeds of *S. aethiopicum* according to treatments T₃ and T₄ in 2020 and T₇ and T₈ in 2021. Overall, the fruit set rate was higher in treatments with flowers visited by *A. mellifera* (T₃ and T₇) than those whose flowers were protected, uncovered and rebagged without visit of insect or any other organism (T₄ and T₈). The difference of the fruit set rate was highly significant between T₃ and T₄ ($\chi² = 20.07; df = 1; P < 0.001$) and between T₇ and T₈ ($\chi² = 24.52; df = 1; P < 0.001$). The value of the fruit set rate due to the foraging activity of *A. mellifera* was 13.04% in 2020 and 17.89% in 2021, with a cumulative mean value of 15.46%.

<table><caption>**Table 3:** Production of eggplant according to treatments T₃, T₄, T₇ and T₈.</caption><thead><tr><th rowspan="2">Years</th><th rowspan="2">Treatments</th><th rowspan="2">NFS</th><th rowspan="2">NFF</th><th rowspan="2">FR (%)</th><th colspan="2">NSF</th><th rowspan="2">TNS</th><th rowspan="2">NNS</th><th rowspan="2">% NS</th></tr><tr><th>m</th><th>s</th></tr></thead><tbody><tr><td rowspan="2">2020</td><td>T₃</td><td>182</td><td>180</td><td>98.90</td><td>401.10</td><td>110.58</td><td>70194</td><td>68745</td><td>97.94</td></tr><tr><td>T₄</td><td>100</td><td>86</td><td>86.00</td><td>363.36</td><td>106.59</td><td>31249</td><td>28240</td><td>90.37</td></tr><tr><td rowspan="2">2021</td><td>T₇</td><td>180</td><td>175</td><td>97.22</td><td>396.07</td><td>125.42</td><td>66937</td><td>65136</td><td>97.31</td></tr><tr><td>T₈</td><td>114</td><td>91</td><td>79.82</td><td>373.10</td><td>130.01</td><td>33953</td><td>31067</td><td>91.50</td></tr></tbody></table>

NFS: number of flowers studied; NFF: number of fruits formed; FR: Fruiting rate; NSF: number of seeds/fruit; TNS: total number of seeds; NNS: number of normal seeds; %NS: percentage of normal seeds; T₃ and T₇: flowers protected then uncovered, visited once by *Apis mellifera* and reprotected; T₄ and T₈: flowers bagged then uncovered and rebagged without visit by insect or any other organism; m: mean; s: standard deviation.

From the same **table 3**, the mean number of seeds per fruit was higher in treatments T₃ and T₇ than in treatments T₄ and T₈. The difference between the mean number of seeds per fruit from both treatments was highly significant in 2020 (*t* = 2.81; *df* = 264; *p* < 0.01) and not significant in 2021 (*t* = 1.33; *df* = 264; *p* > 0.05). The deduced mean number of seeds per fruit for eggplant which resulted from the floral activity of *A. mellifera* was 7.72% in 2020 and 5.97% in 2021, with a cumulative mean value of 6.84%.

The percentage of normal seeds was less important in bagged clusters visited by *A. mellifera* than in flowers protected, uncovered and rebagged without visit of insect or any other organism of corresponding treatments. The *A. mellifera*' floral activity was responsible for the percentage improvement of normal seeds by 9.41% in 2020 and 5.80% in 2021, with a cumulative result of 7.60% for both experiments.

## DISCUSSION

Our findings on the honeybee pollination of eggplant in Dang are once more the confirmation of the mixed reproduction mode autogamy-allogamy characterizing the crop and which is globally consistent with previous information on plant species of the family Solanaceae (Salunkke *et al.*, 1987; Charrier *et al.*, 1997; Smith and Knapp, 2002). Moreover, previous results on the Solanaceae pollinator interactions corroborate the importance of bee species as prominent visitors and efficient pollinators of Solanaceae species. According to Shanika *et al.* (2017), the Solanaceae family is among plant families which are pollinated by bees. In Western Belize (Centre America), seven
Solanaceae species belonging to both genus *Solanum* L., 1753 (*S. erythrotrichum*, *S. lanceifolium*, *S. rudepannum*, *S. cordovense*, *S. nudum*) and *Lycianthes* (*L. hypoleuca* and *L. gorgonea*) were mentioned to be pollinated exclusively by 17 different bee species belonging to Colletidae, Halictidae and Apidae families (Smith and Knapp, 2002). In Oklahoma (Norman), several species in the genus *Bombus* Latreille, 1802 were the primary pollen vector of *S. rostratum* (Solís-Montero, 2013). In Kenya, Gemmill-Harren and Ochieng (2008) identified two native bee species namely *Macronomia rufipes* Smith, 1875 and *Xylocopa caffra* L., 1767 as effective pollinators of *S. melongena*. Oyelana and Ogunwenmo (2012) highlighted the implication of wild bee species *Megachile latimanus* Thomas Say, 1823 in the pollination of *S. aethiopicum* in Nigeria. In Britain, Solanaceae were predominantly pollinated by bees and flies (Edmonds and Chweya, 1997). Mamoudou *et al.* (2021) have already shown the outbreak of *A. mellifera* on *S. nigrum* flowers as the main pollinator of this crop in Maroua (Cameroon); moreover, the findings of Kengni *et al.* (2022) are illustrative of the prominence of a Carpenter bee *Xylocopa* sp. as the main visitor and pollinator of *S. aethiopicum* which are not consistent with the present result in the same plant species with honeybees as the principal anthophilous insect. Of the above, there is a difference in terms of the number of insects and their diversity, plants, periods and geographical areas. In all, the floral entomofauna can vary from plant species to plant species inside the same botany family, for a given plant species from year to year, and for the same year from season to season or site to site (Klein *et al.*, 2007; Ollerton *et al.*, 2011).

The result in exclusively pollen-feeding behavior of *A. mellifera* in the flowers of *S. aethiopicum* is related to the absence of nectar production by this plant species as already ascertained by Mein (2021). Our results highlighted a contrast with those of Mamoudou *et al.* (2021) which are indicative of the dominance of pollen harvesting on the nectar foraging by *A. mellifera* in *S. nigrum* flowers at Meskine (Maroua, Cameroon). The pollen collection by honeybee workers was higher between 8 and 9 a.m which is within the daily period of the highest availability of pollen in the flowers of *S. aethiopicum*.

During their floral activity on *S. aethiopicum*, workers commonly scrabbled and trigged anthers and thus could increase self-pollination of the flowers visited. Visiting a given flower, honeybee individuals were dusted with pollen grains of *S. aethiopicum*. During a floral trip, the high values of the foraging speed which was relatively up to 5 flowers/minute are illustrative of the implication of foragers in the cross-pollination of the flowers visited. Moreover, as a social bee, the pollination ethology of *A. mellifera* workers, which is related to the important number of congeners inside a colony and the ability of explorers to communicate with and recruit several individuals toward an interesting source of booty (Louveaux, 1984) is justificative of the high mean value of the honeybee density on *S. aethiopicum* flowers. This influx of *A. mellifera* foragers visiting eggplant flowers for pollen harvesting implies that this bee species is one of the best pollinator of *S. aethiopicum* in the Adamawa Region of Cameroon. According to Vaissière *et al.* (1996), pollen grains retained by the honeybee hair are efficient for crop pollination.

Overall, the pollination activity of *A. mellifera* impacted positively the reproduction ability and yield improvement of the plant studied. Indeed, the increase of pollen load on the stigmatic surface of each flower visited due to honeybee workers enables the establishment of an important fruiting rate and seed set in open-pollinated flowers comparatively with flowers of *S. aethiopicum* which were bagged to avoid insect visits. Several other studies on plant-pollination networks highlighted the positive influence of anthophilous insect species in increasing fruit and seed production worldwide. A quantitative assessment of the increase in production due to pollinating insects on cotton is known to be 53% in India (Mahadevan and Chandy, 1957). The honey bee increases the yields of *Physalis peruviana* L., 1753 by 7% in Colombia (Chautá-Mellizo *et al.*, 2012). In Cameroon, insects have increased the fruit production of *Physalis minima* L., 1753 by 23% (Djakbé
et al., 2017) and that of *Solanum nigrum* by 16% (Mamoudou et al., 2021).

During the collection of pollen on each flower, *A. mellifera* workers were regularly in contact with the stigma and anthers. They could thus enhance self-pollination, which has been demonstrated in the past by Edmonds and Chweya (1997), by applying pollen of one flower on its stigma. *Apis mellifera* could provide allogamous pollination through carrying of pollen within their hairs, silk, legs, mouthparts, thorax and abdomen, which is then deposited on flowers belonging to a different plant of the same species (geitonogamy) (Edmonds and Chweya, 1997). The positive and significant contribution of *A. mellifera* in the production of *S. aethiopicum* is justified by the action of this bee on the pollination of visited flowers.

## CONCLUSION

In Dang, *S. aethiopicum* has a mixt reproduction mode including the autogamy which predominated the allogamy. Moreover, *A. mellifera* was the main pollen harvester and pollinator on this plant species studied. Honeybee workers enabled the self and cross-pollination to occur, hence helped in boosting the fruiting rate, the mean number of seeds per fruit and the rate of normal seeds per fruit of *S. aethiopicum* by 15.46%, 6.84% and 7.60%. The installation of *A. mellifera* colonies at the vicinity of *S. aethiopicum* fields is recommended to increase fruit quantity and seed production, as well as to improve pollen production as a hive product.

## Acknowledgments

The authors thank all those who facilitated this work, especially the University of Ngaoundéré which provided us the plot for experiments.

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