Visiting behaviour of Moringa oleifera flowers by potential insect pollinators

doi:10.21203/rs.3.rs-3949740/v1

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Visiting behaviour of Moringa oleifera flowers by potential insect pollinators

https://doi.org/10.21203/rs.3.rs-3949740/v1

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The influence of potential insect pollinators is decisive in the fruiting process of many cross-pollinated plants. The aim of this study was to determine the behaviour of potential pollinating insects visiting Moringa oleifera flowers. Collections were carried out from July to September 2018 and 2019, followed by monitoring of the behavior of potential insect pollinators from July to September 2020 in the Sahelian, North Sudanian and South Sudanian zones. The methodology consisted in the use of a Fauchoir net for the exhaustive collection of insects visiting Moringa. The results revealed that a total of 50 species of pollinating insects divided into 25 families and three orders (Hymenoptera, Diptera and Lepidoptera) were identified on the basis of the presence of body hairs on Moringa. Of these, nine insect species collect both nectar and pollen. These are : Xylocopa violacea (L.), Anthophora plumipes (Pallas, 1772), Apis mellifera (L.), Xylocopa pubescens (Spinola, 1838), Pollenia rudis (F.), Alophora hemiptera (F.), Syrphus ribesii (L.), Danaus chrysippus (L.) and Pieris rapae (L.). The times of day when pollinating insects appear on Moringa flowers vary from species to species. The abundance of these pollinators and the duration of their presence on the flowers vary according to geographical area and pollinator species. Hymenoptera are the dominant pollinators in Moringa plantations.

potential pollinators

flowers

floral resources

behavior

climatic zones

Moringa oleifera Lam. originated in northwest India (Foidl et al. 2001) and is now cultivated throughout Africa. Fruit yields are still low, despite heavy flowering. Earlier work presented Moringa as a cross-pollinated species, although self-pollination is also possible (Muluvi et al. 2004). Moringa flowers are pollinated by several types of insects mainly from the order Hymenoptera in India (Bhatnagar et al. 2018; Bhattacharya and Mandal 2004; Jyothi et al. 1990).

The abundance, diversity and frequency of these floral visitor insects depend on environmental factors such as climatic parameters (temperature variability and humidity (Taimanga & Tchuenguem 2018) and habitat (Goulson et al. 2015). Climate change would modify the relationships between plants and their insect pollinators, both locally and regionally (Chagnon 2008), while an insufficient number of pollinators due to habitat fragmentation would greatly reduce or nullify fruit yields (Taimanga & Tchuenguem 2018; Tchuenguem 2005; Vaughton et al. 2010).

In order to improve fruit production, detailed knowledge of plant pollination ecology is needed. Such scientific information is lacking not only for Moringa oleifera but also for most tropical tree species (Bawa, 1989; Zhang et al. 2018). Yet our field observations have shown that Moringa oleifera flowers attract several visiting insects. However, we do not know their contribution to the transport of pollen grains on the stigma of the species' flowers, nor their relationship with their environment in the climatic zones in Burkina Faso. Another fundamental aspect to be taken into account in pollination ecology is the flower-visiting behaviour of insects, notably the floral resources consumed, and the period, number and duration of floral visits. It is known that populations of pollinating insects are guided by the floral resources they seek, the quantity of which may vary according to the rhythm of foraging during the day (Diallo 2001). In the case of Moringa oleifera, in addition to pollinators, few studies are known about their floral visiting behavior. Knowledge of the daily distribution of visits and the resource sought on the flower, as well as the number and duration of pollinator visits, will enable us to gain a better understanding of the existing relationships between pollinators and the flower, and to highlight the existence of any interspecific competition for floral resources.

2.1. Study site

In this study, we concentrated on climatic zones where the species is actually grown in plantations. These are the Sahelian zone, the North Sudanian zone and the South Sudanian zone of Burkina Faso (Guinko, 1984). In each climatic zone, two Moringa oleifera plantation plots were selected.

In the Sahelian zone, Moringa plantations were located in the villages of Poukma and Goinré. In the North Sudanian zone, the study took place in the Moringa plantations of Ouagadougou and Kalzi in the rural commune of Komsilga. In the South Sudanian zone, the study took place in plantations located in the villages of Kouakoualé and Toukoro. All these plantations belong to grower partners of the WANNPRES (Western Africa Network of Natural Products Research Scientists) network. Table 1 shows the characteristics of the sites and the names of the partner growers.

Table 1

The various localities of the selected sites, the geographical coordinates, the areas of the plantations and the partner-producers involved, members of WANNPRES/Burkina Faso.
Climate zone	Site	Latitude	Longitude	Plantation area	Spacing planting	Age (years)
Sahelian	Goinré	13°33'19,7''N	2°25'16,2"W	9000 m²	2mx2m	5
Sahelian	Poukma	13°34’96,6’’N	2°25’29,8’’W	5000 m²	2mx2m	5
Northern Sudanian	Ouagadougou	12°37'84,2''N	1°50'38,7''W	2625m²	2mx2m	4
Northern Sudanian	Kalzi	12°18'48,2''N	1°64'60,2''W	40 000 m²	2mx2m	6
southern sudanian	Kouakoualé	11°01’31,7''N	4°14'38,4''W	15 000 m²	2mx2m	4
southern sudanian	Toukoro	11°12'02,3''N	4°14'38,4''W	5000 m²	2mx2m	5

2.2 Plant material

In the study sites, the work was carried out in fruiting Moringa plantations, at least two years old, under organic cultivation (without synthetic pesticides or chemical fertilizers). Producers' main objective in plantation orchards is seed production. We opted to work in plantations where silvicultural practices are based on the use of organic fertilizers for field improvement and plant maintenance, so as not to influence the presence of flower-visiting insects. Moringa fields were either monospecific or in association with rainfed crops such as sorghum and cowpea.

2.3 Method

2.3.1. Collection of floral visitor insects

Collections of Moringa floral visitor insects were carried out from July to September in 2018 and 2019 respectively at all study sites. This time of year corresponds to full Moringa flowering in Burkina. The method used is the swath net method described by Diallo et al (2014); Goldingay et al (1991) and Zhang et al (2018) to collect diurnal insects. It involves moving around with a mowing net and capturing all floral visitor insects encountered. This technique targets only flower-visiting insects by mowing. The frequency of collection is 10 days a month on sunny days without strong winds.

2.3.2. Identification of pollinating insects

The methodology used was based on those adopted by Lamien et al. (2008); Tankoano (2012); Diallo et al. (2014); Dao et al (2014) when identifying potential pollinators of species in the Sudano-Sahelian zone based on their diet and ability to carry pollen grains on their bodies. The visiting insects we collected in 2018 and 2019 were used to search with a binocular loupe for the actual presence of hairs on their abdomen and the pollen basket on their hind legs. These potential pollinators were then observed in the field to determine their flower-visiting behavior by determining the time of day (or period) of their visits, the type of floral resources sought during their visits (pollen and/or nectar) and the number and duration of floral visits. To estimate visiting behavior, a study sample of 10 trees and 10 blooming flowers per tree, for a total of 100 blooming flowers, were randomly selected on each sampling date for this study. Three time slots per day were defined to account for visitors in the morning hours (6 am to 9 am), the hot hours (10 am to 3 pm) and the evening (4 pm to 6 pm) (Diallo 2001; Dao 2012). Observations were made during the first week of July and August 2020, corresponding to the species' peak flowering period. Two to three passes of 10 minutes/tree during each time slot were made. For each pass, the floral resources visited (nectar and/or pollen), the duration and the number of visits were noted. An insect that buries its proboscis or head in a flower is a nectar seeker; if, using its legs and mandibles, it scratches the anthers, it is a pollen seeker (Taimanga & Tchuenguem 2018). The duration of pollinator visits corresponds to the time it takes the insect to collect the floral resource (pollen and/or nectar) from a flower (Tchuenguem 2005). It was recorded using a stopwatch.

2.4. Statistical analysis

We calculated the relative abundance of pollinators collected by species, family and order in the climatic zones throughout the study period. Next, a data matrix was drawn up based on the presence (noted as 1) or absence (noted as 0) of each species, family and order of insect at each passage. This matrix enabled us to calculate the number of insect species, families and orders present over the course of the study and according to the time of day (morning, warm hours or midday and evening or dusk). To obtain the presence rate, we calculated the percentage of visits by pollinating insects in relation to the total number of visits by time of day (morning, midday and evening).

3.1 Identification of potential insect pollinators

Table 2, shows the potential pollinating insects among floral visitors, those with the ability to carry pollen on their bodies. A total of 50 species from 25 families and three orders (Hymenoptera, Diptera and Lepidoptera) have been identified based on the presence of body hair (Dao et al. 2014; Diallo et al. 2014; Lamien et al. 2008; Tankoano 2008). According to these authors, insects without body hair (pasterns and abdomens) are poorly adapted to transporting pollen from one flower to another. A total of 21 species of potential pollinating insects were identified, common to all three climatic zones. These are : Musca domestica L., Stomoxys calcitrans L., Pollenia rudis F., Plastystoma seminationis F., Alophora hemiptera F., Gymnochaeta viridis F., Syrphus ribesii L., Leucania impure (Hübner, 1808), Arctia caja L., Pieris rapae L., Danaus chrysippus L., Vespila vulgaris L., Anthophora hispanica F., Anthophora plumipes (Pallas, 1772), Apis mellifera L., Bombus hypnorum L., Hypolimnas misippus L., Sphecodes spinolosus (Hagens,1875)., Xylocopa pubescens (Spinola, 1838), Xylocopa confusa (Perez, 1901) and Xylocopa violacea (L.). Species specific to the northern Sudanian zone include Lucilia Caesar L., Dasypholia cyanella (Meigen, 1826) and Megachile xanthoptera S., while those in the Sahelian zone include Eristalis tenax L., Chelostoma florisomne L., Vespa philippinensis (Saussure 1854), Stelis pintulatissima (Kirby, 1802)., Calliopum aeneum (Fallen 1820.) and Bombus agrillaceus ( Scopoli, 1763). In the southern Sudanian zone, potential pollinators include Ammophila sabulasa L., Pemphredon lugubris F., Sceliphron destillatorium (Illiger, 1807) and Anoplius marginatus (Say, 1824).

Table 2

Potential insect pollinators of Moringa in the three climatic zones
Insect order	Family	Scientific name	Climate zone
Hymenoptera	Apidae	Bombus agrillaceus (Scopoli, 1763)	S
	Megachilidae	Stelis pintulatissima (Kirby,1802)	S
	Vespidae	Vespa philippinensis (Saussure, 1854)	S
	Megachilidae	Megachile xanthoptera F.	NS
	Pompilidae	Anoplius marginatus (Say, 1824)	SS
	Sphecidae	Pemphredon lugubris F.	SS
	Sphecidae	Ammophila sabulasa L.	SS
	Sphecidae	Sceliphron destillatorium (Illiger, 1807	SS
	Apidae	Eucera longicornis L.	S,NS
	Braconidae	Apanteles glomeratus L.	S,NS
	Vespidae	Polistes grallicus L.	S,NS
	Megachilidae	Chelostoma florisomne L.	S,NS
	Vespidae	Polistes fuscatus F.	S,SS
	Apidae	Anthophora pilipes F.	SS,NS
	Apidae	Amegilla cingulata F.	SS,NS
	Apidae	Xylocopa albifimbria (Vacahl 1898)	SS,NS
	Ichneumonoidea	Agriotypus armatus (Curtis, 1832)	SS,NS
	Colletidae	Colletes succinctus L.	SS,NS
	Apidae	Apis mellifera L.	S,SS, NS
	Apidae	Bombus hypnorum L.	S,SS,NS
	Apidae	Xylocopa confusa (Perez, 1901)	S,SS,NS
	Apidae	Anthophora plumipes (Pallas, 1772)	S,SS,NS
	Apidae	Xylocopa violacea L.	S,SS,NS
	Apidae	Sphecodes spinolosusn (Hagens,1875)	S,SS,NS
	Apidae	Xylocopa pubescens (Spinola, 1838)	S,SS,NS
	Apidae	Anthophora hispanica F.	S,SS,NS
	Vespidae	Vespila vulgaris L.	S,SS,NS
Lepidoptera	Yponomeutidae	Yponomeuta padella L.	SS,NS
	Nolidae	Nola confusalis (Herrich-Schäffer, 1847)	SS,NS
	Pieridae	Nepheronia argia F.	S,NS
	Lycaenidae	Polyommatus icarus (Rottemburg, 1775)	S,NS
	Nymphalidae	Danaus chrysippus L.	S,SS,NS
	Pieridae	Pieris rapae L.	S,SS,NS
	Arctiidae	Arctia caja L.	S,SS,NS
	Noctuidae	Leucania impura (Hübner, 1808)	S,SS,NS
	Nymphalidae	Hypolimnas misippus L.	S,SS, NS
	Syrphidae	Eristalis tenax L.	S
	Calliphoridae	Lucilia caesar L.	NS
	Muscidae	Dasyphora cyanella (Meigen, 1826)	NS
	Lauxaniidae	Calliopum aeneum (Fallen, 1820)	S,NS
	Coelopidae	Coelopa frigida F.	S,NS
Diptera	Oestridae	Gasterophilus intestinalis (De Geer, 1776)	S,SS
	Syrphidae	Volucella zonaria (Poda 1761)	S,SS
	Tachinidae	Alophora hemiptera F.	S,SS, NS
	Syrphidae	Syrphus ribesii L.	S,SS,NS
	Tachinidae	Gymnochaeta viridis (Fallen 1810)	S,SS,NS
	Platystomatidae	Platystoma seminationis F.	S,SS,NS
	Calliphoridae	Pollenia rudis L.	S,SS,NS
	Muscidae	Stomoxys calcitrans L.	S,SS,NS
	Muscidae	Musca domestica L.	S,SS,NS
S = Sahelian zone, SS = Southern Sudan zone and NS = Northern Sudan zone

3.2. Determining flower visiting behavior

The results of observations of the floral visiting behaviour of potential pollinators are presented in Table 3. Two main groups can be distinguished in terms of the number and duration of visits and the floral resource sought. Group 1 is made up of species that seek both pollen and nectar, and whose duration and number of floral visits per unit of time are the greatest. These are Xylocopa violacea,L.; Anthophora plumipes ( Pallas, 1772), Apis mellifera L. and Xylocopa pubescens ( Spinola, 1838) of the order Hymenoptera (Fig. 1), Pollenia rudis F., Alophora hemiptera F.,, Syrphus ribesii L., of the order Diptera (Fig. 2) and Danaus chrysippus L., Pieris rapae L., of the order Lepidoptera (Fig. 3). The second group is made up of other pollen- and nectar-seeking species with a low number of floral visits and short duration. Based on the diversity of floral resources sought, and the high number and duration of visits per unit of time, we have selected the first group of insect species as Moringa's main pollinators. This group comprises nine species belonging to six families and three orders

Table 3

Floral visiting behaviour of potential pollinators (number and duration of visits and floral resources sought)
Scientific name	Average number of visits/hour	Average length of visit (seconds)	Sought-after floral resource
Polyommatus icarus (Rottemburg, 1775)	1	10	Pollen
Pemphredon lugubris F.	2	12	Pollen
Arctia caja L.	3	13	Nectar
Eucera longicornis L.	2	13	Pollen
Dasyphora cyanella (Meigen, 1826)	5	14	Pollen
Colletes succinta L.	4	15	Nectar
Stelis pintulatissima (Kirby, 1802)	4	15	Pollen
Coelopa frigida F.	1	16	Nectar
Calliopum aeneum (Fallen, 1820)	3	16	Pollen
Polistes grallicus L.	4	16	Pollen
Eristalis tenax L.	2	18	Nectar
Nola confusalis (Herrich-Schäffer, 1847)	1	21	Nectar
Leucania impura (Hübner, 1808)	7	21	Nectar
Apanteles glomeratus L.	5	21	Pollen
Xylocopa confusa (Perez, 1901)	5	22	Nectar
Sphecodes spinolosus (Hagens, 1875)	4	22	Pollen
Anthophora pilipes (Pallas, 1772)	5	23	Pollen
Anoplius marginatus (Say, 1826)	4	24	Pollen
Bombus hypnorum L.	6	24	Pollen
Nepheronia argia F.	2	26	Nectar
Chelostoma florisomne L.	4	27	Nectar
Anthophora hispanica F.	7	27	Pollen
Gasterophilus intestinalis (De Geer, 1776)	7	27	Pollen
Lucilia caesar L.	2	28	Nectar
Polistes fuscatus F.	4	28	Pollen
Musca domestica L.	6	28	Pollen
Megachile xanthoptera F.	2	31	Nectar
Yponomeuta padella L.	4	31	Nectar
Ammophila sabulasa L.	3	31	Pollen
Gymnochaeta viridis (Fallen 1810)	5	31	Pollen
Platystoma seminationis F.	8	31	Pollen
Bombus agrillaceus (Scopoli, 1763)	2	32	Nectar
Agriotypus armatus (Curtis, 1832)	3	33	Pollen
Hypolimnas misippus L.	3	33	Pollen
Sceliphron destillatorium (Drury, 1770)	6	33	Pollen
Volucella zonaria (Poda, 1761)	7	34	Nectar
Vespa philippinensis (Saussure, 1854)	5	36	Nectar
Vespila vulgaris L.	2	37	Nectar
Amegilla cingulata F.	3	37	Pollen
Xylocopa albifimbria (Vacahl 1898)	6	43	Nectar
Stomoxys calcitrans L.	7	45	Pollen
Danaus chrysippus L.	9	53	Pollen + Nectar
Xylocopa pubescens (Spinola, 1838)	10	54	Pollen + Nectar
Pollenia rudis F.	11	54	Pollen + Nectar
Anthophora plumipes (Pallas, 1772	8	60	Pollen + Nectar
Pieris rapae L.	8	61	Pollen + Nectar
Xylocopa violacea L.	7	63	Pollen + Nectar
Alophora hemiptera F.	7	67	Pollen + Nectar
Syrphus ribesii L.	9	78	Pollen + Nectar
Apis mellifera L.	10	78	Pollen + Nectar
Megachile xanthoptera F.	2	31	Nectar

3.3. Determining the abundance of the main pollinating insects by climatic zone

Figure 4 and 5 show that while the main pollinating insect species are present in all three climatic zones, their relative abundance varies. In the North Sudanian zone, the most abundant insect pollinators are Syrphus ribesii, Danaus chrisippus Xylocopa violacea and Apis mellifera in 2018 and 2019. In the South Sudan zone, Xylocopa violacea, Xylocopa pubescens and Apis mellifera were the most abundant on Moringa flowers in 2018, while in 2019 Xylocopa pubescens, Xylocopa violacea and Apis mellifera (Hymenoptera) were the most abundant. In the Sahelian zone, Pollenia rudis followed by Anthophora plumipes, all from the order Hymenoptera, were the most abundant in 2018, and in 2019, these are : Alophora hemiptera and Pollenia rudis (Diptera) were the most abundant. In general, the results show that Xylocopa pubescens, Xylocopa violacea and Apis mellifera, all from the order Hymenoptera, are the most abundant on Moringa flowers in the Sudanian (northern and southern Sudanian) zones, while in the Sahelian zone they are Pollenia rudis and Alophora hemiptera (Diptera) and Anthophora plumipes (Hymenoptera).

3.4. Daily distribution of floral visits by the main pollinators

Figure 6 shows that the daily appearance times of pollinating insects on Moringa flowers vary from one species to another. Four groups of pollinating insects can be considered according to their time of appearance on the blooming flower. The first group of pollinators appears in the morning from 06:00 to 09:00 GMT. It is made up of the following species: Anthophora plumipes, Apis mellifera, Xylocopa pubescens, Pollenia rudis, Alophora hemiptera, Danaus chrysippus, Pieris rapae, Xylocopa violacea. The second group is made up of pollinating insects that visit flowers during the warm hours of the day, from 10 a.m. to 3 p.m. GMT. This second group includes Anthophora plumipes, Apis mellifera, Xylocopa pubescens, Pollenia rudis, Alophora hemiptera, Danaus chrysippus, Pieris rapae, Syrphus ribesii. The third group is made up of insects that visit in the evening from 16–18 h, including the following insect species: Anthophora plumipes, Apis mellifera, Xylocopa pubescens, Pollenia rudis, Alophora hemiptera, Danaus chrysippus, Pieris rapae, Syrphus ribesii, Xylocopa violacea. Finally, the fourth group is made up of pollinating insects that visit Moringa all day long. These are : Anthophora plumipes, Apis mellifera, Xylocopa pubescens, Pollenia rudis, Alophora hemiptera, Danaus chrysippus and Pieris rapae.

A species can be pollinated by several types of insects (Diallo et al. 2014). Under the conditions of our study, the results indicate that insect pollinators of Moringa are composed of several species belonging to the orders Hemiptera, Diptera and Lepidoptera. These results confirm the work of Kevan & Baker (1983), Tankoano et al. (2012) and Muhl et al. (2013) who pointed out that in entomophilic pollination, these 03 insect orders are the most cited as pollinators of woody species. The latter have the ability to transport pollen on their abdomens or on their proboscis (Thione 2000). Insects of the Apidae family (Hymenoptera), for example, send their proboscis all around the corolla in search of nectar. By sucking nectar from the nectariferous disc or cleaning their bodies with their legs, pollen is easily transported or deposited on the stigma (Thione 2000).

In relation to previous work carried out on Moringa pollinators, our results invalidate those of Krieg et al. (2017) who had identified only the Hymenoptera as the only insect pollinator order of Moringa at Dano in the South Sudanian zone of Burkina Faso. No insect species from the orders Lepidoptera and Diptera had previously been identified as pollinators in the South Sudanian zone. We can explain our results by the seasonal dynamics of flowering, which would influence the composition of the insects collected. Collecting in two flowering seasons enabled us to cover the maximum number of specimens collected, unlike the Dano collections, which were carried out in a single flowering season.

Bhatnagar et al. (2018) had surveyed the pollinators of M. oleifera in India, mainly composed of insects of the orders Lepidoptera and Hymenoptera. According to these authors, no insect species of the order Diptera had previously been identified as pollinators in India in the species' country of origin. These results also differ from our own, carried out in all three climatic zones. This difference with previous work on Moringa can be explained by the nature of the habitats concerned. Our previous work in Dano was carried out in a monospecific Moringa field located on the outskirts of the town of Dano, whereas our work was carried out in plantations associated with crops located on the outskirts of major urban centers. Compared with the others, our Moringa plantations are in association with several crop species whose rainy-season flowering takes place at the same time as Moringa. This could encourage greater interaction between floral visitors and increase the capture rate on Moringa flowers. This explanation is also in line with the work carried out in the Mount Carmel National Reserve in Israel (Mediterranean climate) by Potts et al. (2003), who found that the specific diversity of visiting insects was high when the floral resource was available in the environment.

Other groups of researchers, such as Schueps et al. (2011) and Mudri-Stojnić et al. (2012), on the contrary, emphasized the immediate environment of plantations and the degree of connectivity between them. For them, when the connectivity of plantations through the movements of pollinating insects (gene flow exchanges) is interrupted because they are isolated as a result of anthropogenic disturbance, this reduces pollinator diversity and the maintenance of plant species populations over the long term. Our study shows that Moringa pollinators visit flowers at different times of the day. A. mellifera (Hymenoptera) visits flowers more frequently in the morning. Similar results were obtained on tamarind by Diallo et al. (2014) in the northern and southern Sudanian zones of Burkina Faso. The presence of Apis early in the morning on flowers, would coincide with the maximum production of nectar and pollen, which would constitute their main floral resource sought in flowering plants ( Diallo et al. 2014; Dao et al. 2014). Our study on floral visits confirms the longer duration of visiting time of Apis mellifera (Hymenoptera) compared to other insects (Diallo et al. 2014; Bhatnagar et al. 2018). This is due to the availability of floral resources produced. Indeed, Bhatnagar et al., (2018) found that the duration of visits to flowers is correlated with the quantity and quality of nectar. The abundance and frequency of A. mellifera visits had also been reported on the flowers of Piliostigma reticultum (Dao et al. 2014), Tamarindus indica (Diallo et al. 2014), Vitellaria paradoxa (Lamien et al. 2008); Ziziphus mauritiana ( Tankoano et al. 2012); Parkia biglobosa (Lamien et al. 2011; Sina 2006). This interaction with several species in the same environment is explained by the fact that in honey bees, the forager is able to memorize and recognize the shape, color and odor of several types of flowers visited during previous foraging trips (Palumbo 2019; Wright et al. 2002).

The daily distribution of pollinator visits shows that Syrphus ribesii visits the Moringa flower during the hot hours of the day for nectar and pollen (Speight et al. 2007), but also for aphid predation (insects of the order Hemiptera) ( Sarthou 1996). Under these conditions, we believe that they come to Moringa for two reasons. Apart from their role as pollinators, they also pursue insects of the Hemiptera order (aphids) which seek shelter to avoid hot weather or flee predation. This means that Moringa could be a place of refuge and shelter for certain aphids.

In addition to these roles played by Moringa flowers, we also believe that the presence of S. ribesii on Moringa is linked to their reproductive cycle, part of which takes place during the hot hours of the day. For it had already been reported by Haffaressas (2018) that S. ribesii females lay their eggs on trees in gardens, parks or plantations, with hatching and larval emergence taking place under conditions of high temperature and hygrometry.

The study identified around fifty potential pollinators morphologically suited to transporting pollen on the flower stigma. Nine of these potential insect pollinators are considered to be the most important in terms of their flower-visiting behavior. These main insect pollinators are Xylocopa violacea, Anthophora plumipes, Apis mellifera and Xylocopa pubescens (Hymenoptera), Pollenia rudis, Alophora hemiptera and Syrphus ribesii (Diptera), Danaus chrysippus and Pieris rapae (Lepidoptera). They collect both nectar and pollen and spend varying amounts of time on moringa flowers. Xylocopa pubescens, Xylocopa violacea and Apis mellifera (Hymenoptera) Syrphus ribesii (Diptera) and Danaus chrisippus (Lepidoptera) were the most abundant in Sudanian zones, and Pollenia rudis and Anthophora plumipes (Hymenoptera) in Sahelian zones.

Our results confirm the dominance of Hymenoptera pollinators on Moringa. The study highlighted the existence of a distribution of pollinators observed in search of the plant's floral resources. The flowers are permanently visited by all pollinators except Xylocopa violacea and Syrphus ribesii. But Apis mellifera remains the most abundant in the morning, while Xylocopa violacea is the most abundant in the warmer hours of the day.

Conflict of interest declaration:

On behalf of all authors, the corresponding author declares that there is no conflict of interest.

Bawa KS, Buckley DP (1989) Seed ovule ratios, selective seed abortion and mating systems. In: Leguminosae. Advances in legume biology: (eds.) C. Stirton et J. L. Zarucchi. Monographic, Systematic and Botanic. Missouri Botanic Gardens Kew 12(3):243–262
Bhatnagar S, Rathore LS, Khan AU, Sharma N, Kumar B (2018) Record of insect pollinators of Moringa oleifera lam. J Entomol Zool Stud 6(4):389–391
Bhattacharya A, Mandal S (2004) Pollination, pollen germination and stigma receptivity in Moringa oleifera Lam. Grana 4(1):48–56. https://doi.org/10.1080/00173134.2004.11877463
Chagnon M (2008) Causes et effets de déclin mondial des pollinisateurs et les moyens d’y remédier. Fédération Canadienne de La Faune 3(1):70
Dao ECM (2012) Biologie et écologie de la reproduction sexuée d’une Caesalpinioideae (Leguminoseae): Piliostigma reticulatum (D.C.) Hochst. Thèse de Doctorat de l’Université Polytechnique de Bobo-Dioulasso (UPB) / Burkina - Faso; 112P
Dao MCE, Diallo BO, et, Zoungrana CK (2014) Flowering phenology and floral visitors of Piliostigma reticulatum in a tropical dry forest, Burkina Faso. Int J Biol Chem Sci 8(1):237–248
Diallo BO (2001) Biologie de la reproduction et Evaluation de la diversité génétique chez une légumineuse: Tamarindus indica L. (Caesalpinioideae). Univ. Montpellier II. Science et Technique du Languedoc 137P
Diallo BO, Ouedraogo M, Chevallier M (2014) Potential pollinators of Tamarindus indica L. (Caesalpinioideae) in Sudanian region of Burkina Faso. Afr J Plant Sci 528–536. https://doi.org/10.5897/AJPS12.072
Drugmand J (2020) Impact des stress thermique et hydrique sur la croissance, la reproduction et la pollinisation de Fagopyrum esculentum et comparaison de la pollinisation chez deux espèces de Fagopyrum. Université catholique de Louvain. Quinet, Muriel. Thèse, 100P. http://hdl.handle.net/2078.1/thesis:23008
Foidl N, Makkar HPS, et Becker K (2001) Potentiel de Moringa oleifera en agriculture et dans l’industrie, un potentiel de développement des produits du Moringa. Dar Es Salaam, Tanzanie. 20P
Rotheray LE (2015) Les abeilles déclinent en raison du stress combiné des parasites, des pesticides et du manque de fleurs. Am Association Advancement Sci 348(6238):981–989
Haffaressas B (2018) Inventaire et écologie des Syrphidés (Ordre: Diptera) de la région de Guelma. Thèse Doctorat. Université 8 Mai 1945-Guelma.157P.
Jyothi PV, Atluri JB, Subba Reddi C (1990) Pollination ecology of Moringa oleifera (Moringaceae). In Proc. Indian Acad. Sci. (Plant Sci.) (Vol. 100, Issue 1)
Kevan PG, Baker HG (1983) Insects as flower visitors and pollinators. Rev EntomoL 28(4):407–413
Krieg J, Goetze D, Porembski S, Arnold P, Linsenmair KE, Stein K (2017) Floral and reproductive biology of Moringa oleifera (Moringaceae) in Burkina Faso, West Africa. 63–70. https://doi.org/10.17660/ActaHortic.2017.1158.8
Kumar P, Baskaran S, Sundaravadivelan C, Anburaj J, et Kuberan T (2012) Insect visitors of pumpkin, Cucurbita maxima Duch., in relation to temperature and relative humidity. J Agricultural Technol 66(2):37–39
Lamien N, Kabore AK, Tamini Z (2008) Greffage de quatre fruitiers locaux: (Tamarindus indica L., Saba senegalensis (A. DC.) Pichon, Lannea microcarpa Engl. et K. Krause et Sclerocarya birrea (A. Rich.) Hochst au Burkina Faso. Science et Technique, Sciences Naturelles, 30(1), 53–60
Lamien N, Ekué M, Ouedraogo M, et Loo J (2011) Parkia biglobosa, néré. Conservation et utilisation durable des ressources génétiques des espèces ligneuses alimentaires priori. Taires de l’Afrique Subsaharienne. Bioversity Int (Rome Italie) 3(1):11
Mudri-Stojnić S, Andrić A, Józan Z, Vujić A (2012) Pollinator diversity (Hymenoptera and Diptera) in semi-natural habitats in Serbia during summer. Archives Biol Sci 64(2):777–786. https://doi.org/10.2298/ABS1202777S
Muhl QE, Toit ES, Steyn JM, Apostolides Z (2013) Bud development, flowering and fruit set of Moringa oleifera Lam. Horseradish Tree) as affected by various irrigation levels. University, p 35
Muluvi GM, Sprent JI, Odee D, Powell W (2004) Estimates of outcrossing rates in Moringa oleifera using Amplified fragment length polymorphism (AFLP). Afr J Biotechnol 3(2):145–151. http://onlinelibrary.wiley.com/doi/ 10.1002/cbdv.200490137/abstract
Palumbo S (2019) Variation de la qualité des ressources florales des abeilles en milieu agricole. Mémoire en Sciences biologique.Université de Mons, 96 pp
Potts SG (2003) Linking Bees and Flowers: How Do Floral Communities Structure. Pollinator Communities? Ecol 84:2628–2642
Schüepp C, Herrmann JD, Herzog F (2011) Differential effects of habitat isolation and landscape composition on wasps, bees, and their enemies. Oecologia 165, 713–721 (2011). https://doi.org/10.1007/s00442-010-1746-6
Sina S (2006) Reproduction et diversité génétique chez Parkia biglobosa (Jacq.) G.Don. Wagenigen University, Wageningen, The Netherlands. 102pp
Stangler ES, Hanson PE, Steffan.-Dewenter I (2014) Interactive effects of habitat fragmentation and microclimate on trap-nesting Hymenoptera and their trophic interactions in small secondary rainforest remnants. Biodivers Conserv 24(3):634. https://doi.org/10.1007/s10531-014-0836
Taimanga T, Tchuenguem Fohouo F-N (2018) Diversité des insectes floricoles et son impact sur les rendements fruitiers et grainiers de Glycine max (Fabaceae) à Yassa (Douala, Cameroun). Int J Biol Chem Sci 12(1):141. https://doi.org/10.4314/ijbcs.v12i1.11
Tankoano MP (2008) Etude de l’entomofaune et des productions fruitières chez trois variétés indiennes de Ziziphus mauritiana Lam. (Rhamnaceae) introduites au Burkina Faso. Mémoire Cycle ingénieur – Univ-UPB. 90 P No 00-2008/ eau et Forêts (Issue 00)
Tankoano PM, Diallo OB, Ouedraogo SN, Some NA, Noula K, Kalinganire A (2012) Inventaire des insectes nuisibles aux fruits des variétés indiennes de Ziziphus mauritiana Lam. (Rhamnaceae) au Burkina Faso. Fruits 67(3):189–200. https://doi.org/10.1051/fruits/2012012
Tchuenguem FF-N (2005) Activité de butinage et de pollinisation d’Apis mellifera adansonii Latreille (Hymenoptera: Apidae, Apinae) sur les fleurs de trois plantes à Ngaoundéré. (Cameroun): Callistemon rigidus (Myrtaceae), Syzygium guineense var. macrocarpum (Myrtaceae) et Voacan. Thèse de Doctorat d'Etat.Université de Yaoundé I. (Cameroun).103P
Thione L (2000) Biologie de la reproduction et étude de l’impact de l’exploitation des feuilles et des fruits sur la productivité des rôniers. Thèse de troisième Cycle, vol 135. Université Cheick Anta Diop de Dakar
Vaughton G, Ramsey M, Johnson SD (2010) Pollination and late-acting self-incompatibility in Cyrtanthus breviflorus (Amaryllidaceae): Implications for seed production. Ann Botany 106(4):547–555. https://doi.org/10.1093/aob/mcq149
Wright GA, Skinner BD, Smith BH (2002) Ability of honey bee, Apis mellifera, to detect and discriminate odors of varieties of canola (Brassica rapa and Brassica napus) and snopgragon flowers (Antirrhinum majus). J Chem Ecol 28(4):721–740
Zhang J, Lin M, Chen H, Zh Q, Linh VN, Chen X (2018) Floral biology and pistil receptivity of the drumstick tree (Moringa oleifera Lam). Arch Biol Sci 70(2):299–305

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Visiting behaviour of Moringa oleifera flowers by potential insect pollinators

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Abstract

Figures

1. Introduction

2. Materials and methods

2.1. Study site

2.2 Plant material

2.3 Method

2.3.1. Collection of floral visitor insects

2.3.2. Identification of pollinating insects

2.4. Statistical analysis

3. Results

3.1 Identification of potential insect pollinators

3.2. Determining flower visiting behavior

3.3. Determining the abundance of the main pollinating insects by climatic zone

3.4. Daily distribution of floral visits by the main pollinators

4. Discussion

5. Conclusion

Declarations

References

Status:

Version 1