Esther Nadine Otiobo-Atibita, Njoya Moses Tita-Mogho, Dounia Dounia, Champlain Djieto-Lordon & Fernand-Nestor Tchuenguem-Fohouo

Le rôle de l’abeille non-Apis dans la fructification de Abelmoschus esculentus (L) Moench 1794 (Malvales : Malvaceae) à Bambili (Cameroun)

Résumé

Cette étude a été menée à Bambili du 9 janvier au 10 février 2020 afin de déterminer l’impact des visites de l’abeille non-Apis sur la pollinisation et la productivité de Abelmoschus esculentus. Deux traitements ont été réalisés sur 30 plantes sélectionnées au hasard pour chaque traitement. Le traitement n^o1 comprenait des fleurs isolées de visites d’insectes à l’aide de sachets en toile gaze et le traitement n^o2 était constitué de fleurs ensachées limitées à la seule visite de l’abeille sauvage. Le comportement de butinage sur les fleurs et l'efficacité pollinisatrice (taux de fructification, nombre de graines / fruits et pourcentage de graines normales) de cet insecte ont été enregistrés. Les résultats ont montré que le taux de fructification, le nombre de graines / fruits et le pourcentage de graines normales du traitement n^o2 étaient significativement élevés par rapport à ceux du traitement n^o1. L’abeille non-Apis récoltait le pollen et le nectar des fleurs de A.esculentus. Cette abeille sauvage est un pollinisateur efficace car sa visite a augmenté le taux de fructification de 38,53%. L’installation des nids de cette abeille sauvage près des champs de gombo est recommandée pour améliorer la pollinisation et la productivité de cette plante à Bambili

Abstract

Experiments were made to determine the effects of the non- Apis bee visits on the pollination and the productivity of Abelmoschus esculentus from January 9 to February 10, 2020 in Bambili. Two treatments were used on 30 randomly-selected plants for each. These included bagging flowers to avoid any other visits (treatment no1) and bagged flowers limited on a single visit of the non-Apis bee (treatment no2). The foraging behavior on flowers and the pollination efficiency (fruiting rate, number of seeds / fruit and percentage of normal seeds) of that insect species were recorded. Results showed that the fructification rate, the number of seeds per fruit and the percentage of normal seeds of treatment no2 was significantly high than that of treatment no1. The non-Apis bee foraged pollen and nectar of A. esculentus flowers. The insect species was effective pollinator as its visit increased the fruiting rate by 38.53%. The nests attraction of this wild bee is recommended to improve the pollination and the productivity of gumbo in Bambili.

Table des matières

Reçu le 12 janvier 2021, accepté le 17 août 2021

L’article est distribué suivant les termes et les conditions de la licence CC-BY (http://creativecommons.org/licenses/by/4.0/deed.fr)

INTRODUCTION

1Pollinators are a key component of global biodiversity, providing vital ecosystem services to crops and wild plants (Gallai et al., 2009) and their role in many plants is well known throughout the world (Jacob-Remacle, 1989). Many insects visit flowers from which they obtain carbohydrate and protein food (Pesson & Louveaux, 1984). In turn, they pollinated the visited flowers (Cane, 2002). In natural environments as in agro-ecosystems, insects in general and Apoidea in particular, have a great ecological and economic value because they have a positive influence on agro-food production (Desquesne, 1996). In many crop plant species, the honey bee (Apis mellifera) seems to be the central pollinator insect (Klein et al., 2007) but many techniques are now developed on habitat conservation to maintain the population of natural bees (Torchio, 1990) for the pollination services (Velthuis & Van Doorn, 2006), wellbeing (Gallai et al., 2009) and natural world (Ricketts et al., 2004).

2Abelmoschus esculentus, commonly called okra, lady’s finger or gumbo, is an important crop grown in many parts of the world, especially in tropical including Asia, Central and South America (FAOSTAT, 2008) and sub-tropical countries (Kumar et al., 2010). The plant is a rich source of water, protein, carbohydrates, fiber, calcium, zinc, iron and vitamin A, B and C (Norman, 1992; Justo, 2005). Many insect species forage in the gumbo field as predators, decomposers, parasitoids and pollinators. Honey bees, bumble bees, ants, butterflies and many other pollinating insects forage in the gumbo field due to its attractive golden yellow flowers containing nectars (Bajiya & Abrol, 2017; Nandhini et al., 2018). The crop is cultivated for its edible leaves, buds, flowers and fruits and easy to farm (Angbanyere & Baidoo, 2014). Gumbo is sometimes grown purposely for the seeds because of their high amounts of edible oil (Njoya et al., 2005). The plant species is of considerable economic importance (Njoya et al., 2005; Sawadogo et al., 2006) because the global demand for gumbo is increasing due to the growing health consciousness and its high nutritional qualities as an excellent source of food and bio medicine (reddy et al., 2004) and high financial value (Sawadogo et al., 2006). In Cameroon gumbo occupies a prominent place in the diet, culture and life of many ethnic groups in the Far North Region, North-West Region and West Region. A.esculentus is self-compatible and self-pollination can take place in its hermaphrodite flowers despites the fact that the flowers are insect-pollinated (Al-Ghzawi et al., 2003).

3In Cameroon one of the key objectives of agricultural research is to obtain high and sustainable yields to feed the growing population (DSCE, 2009) but the production of gumbo is low (100,025 tons) (FAO, 2018). This low production is because gumbo crop is suffering from number of biotic (like gumbo parasites) and abiotic factors (like high temperature), including lack of knowledge on the importance of flowering insect pollinators in increasing yields of vegetable crops. Therefore it is important to study the possibilities to increase the production of gumbo. Few published data do exist on the relationships between insect foragers and A.esculentus flowers. Njoya et al. (2005) in Yaounde (Cameroon) observed on preliminary trials that Megachile spp., Halictus spp., Xylocopa spp. and A. mellifera were the main okra anthophilous insects; Azo’o et al. (2011) in Maroua-Cameroon found that Eucara macrognatha Gerstaecker, 1870 and Tetralonia fraternal Friese, 1911 were the two main bee visitors and were effective gumbo pollinators; Amada et al. (2018) in Yaounde found out that Xylocopa olivacea Fabricius, 1787,Synagris cornuta Linnaeus, 1758 and the ants were the most frequently insect species pollinators of A. esculentus; Pando et al. (2020) in Maroua and Otiobo et al. (2020) in Bambili found that Lipotriches collaris Vachal, 1903 was the most pollinators of A.esculentus. Following the lack of complete data on the relationship between A.esculentus and its floral entomofauna, the emergency to know the crop-plant pollinators for their conservation and the necessity to produce higher quantity seeds to meet their various uses, it is important to carry out further researches on gumbo in order to complete the useful available data. Thus it’s necessary to conduct investigations on the relationships between A.esculentus and their flowering insects in Bambili, North West Region of Cameroon, to increase the existing data for Cameroon. The main objective of our research was to contribute to the knowledge of the importance of a non-Apis bee, known to be the most prevalent for the insect visiting gumbo in Bambili. Specifically, our study was aimed at evaluating the impact of a single visit of the non-Apis bee on A.esculentus pollination and fructification.

MATERIALS AND METHODS

Study site

4This experiment was carried out from January 9 to February 10, 2020. The study was carried out in Bambili (6°00’29’’N 10°25’90’’E and 1430 m above sea level), Tubah Sub Division, Mezam Division, in the North West Region of Cameroon during the dry season. The climate is of the tropical monsoon type with two seasons, namely the rainy season (mid-March to mid-October) and the dry season (mid-October to mid-March) (Neba & Eze, 2004). The annual average precipitation ranges from 1770 mm to 2824 mm, the mean annual temperature is 20°C and the mean annual relative humidity is above 85% (Abdoul et al., 2008).

Biological Material

5The bee material was represented by the population of the non-Apis bee (figure 1) which came from the ground nests present on the study site and the plant material was made up of seeds of A.esculentus (figure 2) bought from “Farmers Pharmacy” located at “Three corners” Bambili.

Figure 1 : The non-Apis bee captured on Abelmoschus esculentus flower

Figure 2 : Dried seeds to be planted (A) and an open flower (B) of Abelmoschus esculentus (©Otiobo, 2020)

METHODOLOGY

6The methodology used was modified from that of Azo’o et al. (2012). An experimental plot of 10 m long and 9 m wide was selected for the study. It was cleared and cleaned with a cutlass on 20 September, 2019. Then using a digger and a hoe, the soil was tiled and 10 ridges of 3 m long by 1 m wide and 0.3 m high each were formed. The distance between ridges was 0.5 m wide. The vegetation near A.esculentus field was represented by crops, ornamental plants and native plants.

7Prior to planting, fowl droppings were mixed with the ground and put in holes destined for each gumbo plant. Two okra seeds were then deposited in each hole on a row of three lines while maintaining a gap of 0.5 m between two holes. Watering was done daily between 4-6 pm to prevent drying. From germination (13th October, 2019) to the opening of the first flowers (27th December, 2019), weeding was done manually every two weeks to maintain ridge weeds-free.

8Direct observations on flowers were made daily from January 9 to February 10, 2020 within the blooming period and between 11:00 am and 12:00 pm (local time) since previous observations indicated that gumbo flowers were fully visited by the non-Apis bee species for the whole day with a peak of activity between 11:00 am and 12:00 pm (Otiobo et al., 2020). At most five specimens of the wild bee species were captured globally with an insect net and were conserved in a box containing 70% of ethanol for future taxonomy. Bee identifications were done by Dr. Dounia, Laboratory of Zoology, Higher Teacher Training College, University of Yaounde I, using identification books (Delvare & Aberlenc, 1989; Borror & White, 1991; Eardley et al., 2010). To assess pollination effectiveness, we used random samples of 30 experimental plants for each of the two treatments including autonomous self-pollination (ASP) and single bee visit (SBV).

9In autonomous self-pollination (ASP) (treatment no1), flower buds were isolated with gauze bags of 1mm² mesh (figure 3) a day before anthesis to prevent anthophilous insect visitation and airborne pollen flow the following day. The flower and the equivalent plant were labeled.

Figure 3 : Abelmoschus esculentus plant showing flowers protected with gauze bags (©Otiobo, 2020)

10In single bee visit (SBV) (treatment no2) a team of four observers was positioned in the study field. The observers were placed 2 m away from a newly open flower of a given plant from 11:00 am (local time) before the arrival of bee foragers. Each flower was monitored until it received a single visit by the non-Apis bee.

11The floral product harvested (nectar or pollen) was registered and this was done on the basis of the foraging behavior of the non-Apis bee. Nectar harvesters were seen going on the bottom of the flower and gathering this product at the level of the nectary while pollen gatherers directly scratched the anthers with mandibles or legs.

12Moreover, the duration of bee visits was recorded by the observer using a stopwatch. After a bee visit, the flower was bagged with a gauze bag until the next day to avoid any additional insect visitation (Vaissière et al., 1996; Gingras et al., 1999) after which the flower and the equivalent plant were also tagged. For all treatments, only the first flower at the base of the plant was considered. Two weeks after anthesis, each fruit was harvested and tagged for future analysis according to Tchuenguem et al. (2004):

13- The contribution (Fr) of the non-Apis bee in the fruiting was calculated as follows: Fr = {[(Fr2- Fr1) / Fr2] x 100} where Fr2 were the fruiting rate in bagged flowers visited exclusively by the non-Apis bee (treatment no2) and Fr1 were the bagged flowers (treatment no1).

14- The percentage of the number of seeds per fruit (Ps) due to the influence of the non-Apis bee was calculated as follows: Ps = {[(s2 - s1) / s2] x 100} where s2 and s1 were the mean number of seeds per fruit in treatment no2 and no1.

15- The percentage of normal seeds (Pns) due to the influence of the non-Apis bee was calculated as follows: Pns = {[(ns2 - ns1) / ns2] x 100} where ns2 and ns1 were the percentages of normal seeds in treatment no2 and no1.

Data analysis

16The data was processed using descriptive statistics (calculation of means, standard deviations and percentages) and two tests: student’s (t) for the comparison of means of two samples and chi-square (x2) for the comparison of percentages on Microsoft Excel 2010.

RESULTS

Foraging ethology

17The non-Apis bee selectively visited the open flowers of A.esculentus. The wild bee comes into contact with the flower from above, either on the stamens and the stigma, or on the corolla. Subsequently, the bee scratches the anthers to collect pollen (figure 4). The forager temporarily stops the pollen harvest at the anthers and then lands on the corolla to complete the collection of the pollen collected. They could therefore intervene directly on self-pollination, by putting the pollen of a flower on its stigma. All the 30 (100%) single visits of the non-Apis bee were with stigmatic contact. The activity of this wild bee observed foraging on gumbo flowers was for pollen and nectar gathering base to its foraging behavior. The mean duration of a bee visit was 10.87s (ESM = 6.26; n = 30) for the collection of nectar and 11.33 s (ESM = 4.85; n = 30) for the collection of pollen. The difference between these two averages is significant (t = - 1.21; p<0.001)

Figure 4: The non-Apis bee collecting pollen in a flower of Abelmoschus esculentus (©Otiobo, 2020)

Impact of the non-Apis bee on Abelmoschus esculentus yields

18During pollen and nectar harvest, the non-Apis bee species were in regular contact with the anthers and stigma. Thus this insect increased the pollination possibilities of this plant species. Table 1 gives the fruiting rate, the number of seeds per fruit and the percentage of normal seeds in treatment no1 (autonomous self-pollination) and treatment no2 (single non-Apis bee visit). The fruiting rate was 70% in treatment no1 and 83.33% in treatment no2. The difference between this percentage and that obtained in treatment no1 is not significant (χ2 = 1.49; p˃0.05).

19The average number of seeds per fruit was 14 in treatment no1 and 21 in treatment no2. The difference between this average and that obtained in treatment no1 is highly significant (t = -3.80; p<0.01).

20The percentage of normal seeds was 75.36% in treatment no1 and 86.19% in treatment no2. The difference between this percentage and that obtained in treatment no2 is very highly significant (χ2 = 19.86; p<0.001). Thus, the flowers protected then visited exclusively by the non-Apis bee gave higher fruit and grain yields than those of protected and unvisited flowers.

Table 1: Parameters associated to the production of Abelmoschus esculentus according to treatments

Parameter	ASP	SBV	- Comparison of fruiting rates: SBV / ASP: χ2 = 1.49 (df = 1, p˃0.05, NS); - Comparison of the average number of seeds / fruit: SBV / ASP: t = -3.80 (df = 58, p<0.01, HS); - Comparison of the percentages of normal seeds: SBV / ASP: χ2 = 19.86 (df = 1, p<0.001, HS)
NFS	30	30
NFF	21	25
FR (%)	70.00	83.33
Seed / fruit	14 ± 7	21 ± 7
TNS	418	630
NNS	315	543
NS (%)	75.36	86.19

NFS: number of flowers studied; NFF: number of fruits formed; FR: fruiting rate; TNS: total number of seeds; NNS: number of normal seeds; % NS: percentage of normal seeds; HS: highly significant; NS: not significant; ASP: protected flowers; SBV: protected flowers and having been visited exclusively by the non-Apis bee.

DISCUSSION

21In this work, it is observed that self-pollination in gumbo plant allows the production of fruits and seeds without any pollen deposition by anthophilous insects. Our results agreed with other reports (Al Ghzawi et al., 2003; Azo’o et al., 2011, 2012). As pollen grains of gumbo are very large (Vaissière & Vinson, 1994) and are not wind borne (Mc Gregor, 1976), it is the natural contact between the uppermost anthers and the lower part of the stigma that enables self pollination (Hamon & Koechlin, 1991). Although yields are higher with the presence of pollinators such as the non-Apis bee as it is showed in Table 1.

22Gumbo floral products attract various insect species in natural conditions especially the non-Apis bee which collects both nectar and pollen on gumbo flowers in our study area. This result is in agreement with those obtained by Perera & Karunaratne (2019) in Sri Lanka with Lithurgus atratus. L. collaris was recognized as the major insect pollinator in Maroua (Cameroon) (Pando et al., 2020). The genus Apis with the species cerana was identified as the main A.esculentus pollinator in India (Crane, 1991). Eucara macrognatha and Tetralonia fraterna were collected on the flowers of A.esculentus (Pauly, 1984) in some tropical country of Africa and in Cameroon particularly (Azo’o et al., 2011). Amada et al. (2018) in Yaounde (Cameroon) found out that Xylocopa olivacea, Synagris cornuta and the ants were the most frequently insect species pollinators of A. esculentus. Toni et al., (2020) in the Ketou community (South Benin found that E.macrognatha was the most effective pollinator of the gumbo. Honeybees were found to be the main insect pollinator in the forest Region of Ghana (Angbanyere & Baidoo, 2014). This attractiveness could be due to the availability in great quantity of those floral products. Moreover, gumbo is a plant that produces nectar and pollen able enough to substantially contribute to the maintaining of the nutritional needs of the wild and domesticated bee species.

23The harvesting of nectar by the non-Apis bee could be due to high concentration in total sugars considering the range of 15 to 75% for numerous plant species (Proctor et al., 1996). According to Phillipe (1991), bees are generally constant on a plant species when the concentration in sugars of its nectar is more than 15% and Azo’o et al. (2012) found in their study that the mean value of the sugar content of the nectar in A.esculentus was 21.74%. Pollens have been collected by the non-Apis bee because they need them for food; moreover pollens are a rich source of protein (Pesson & Louveaux, 1984). This would be an explanation of the good attachment of this bee to the pollen and/or nectar of A.esculentus.

24Individuals from the non-Apis bee spend more than 10 sec visiting a flower. During this time, they frequently contacted the anthers, got the echinate pollen grains in the body hair (Hamon & Koechlin, 1991) and could thereby do pollination with this self pollen before flying off.

25The significant contribution of pollinating insects in pods and seed yield of A.esculentus was found. In Cameroon, Azo’o et al. (2012) showed that A.esculentus flowers produce fewer seeds per pod in the absence of pollinating insects. The weight of insect pollinators played a helpful role during nectar or pollen collection: those insects shook flowers, facilitating the liberation of pollen by anthers for the optimal occupation of the stigma (Klein et al., 2007). This higher productivity of pods and seeds in single non-Apis bee visit when compared with bagged flowers showed that the wild bee visits were effective in increasing pollination. This result is in accordance with that of Azo’o et al. (2012), Amada et al. (2018), Perera & Karunaratne (2019) and Pando et al. (2020) showed the importance of wild bees as the main pollinating insects of this crop.

CONCLUSION

26Abelmochus esculentus is a plant species that benefits from the foraging activity of the non-Apis bee on its flowers despite is capacity of self-pollination. The significant increase in yields of A.esculentus in the presence of the non-Apis bee is the consequence of the foraging activity of these insect species on the pollination of the flowers of the plant studied. Thus the conservation of those wild-bee nests in areas surrounding gumbo crops in bloom is recommended.

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A propos de : Esther Nadine Otiobo-Atibita

A propos de : Njoya Moses Tita-Mogho

A propos de : Dounia Dounia

A propos de : Champlain Djieto-Lordon

A propos de : Fernand-Nestor Tchuenguem-Fohouo