Effect of the Botanical Insecticides on <i>Amegilla</i> Friese, 1897 (Hymenoptera: Apidae) Foraging on the Cowpea Flowers in Dang (Adamaoua, North-Cameroon)

Taimanga; Moise Adamou; Georges Tchindebe; Moukhtar Mohammadou; Ousmana Youssoufa; Boris Fouelifack-Nintidem; Alice Virginie Tchiaze Ifoue; Andrea Sarah Kenne Toukem; Odette Massah Dabole; Oumarou Abdoul Aziz; Abraham Tchoubou-Sale; Sedrick Junior Tsekane; Daniel Kosini; Pharaon Auguste Mbianda; Martin Kenne

doi:doi:10.11648/j.aje.20240803.13

Research Article |

| Peer-Reviewed

Effect of the Botanical Insecticides on Amegilla Friese, 1897 (Hymenoptera: Apidae) Foraging on the Cowpea Flowers in Dang (Adamaoua, North-Cameroon)

Taimanga

, Moise Adamou

, Georges Tchindebe

, Moukhtar Mohammadou

, Ousmana Youssoufa

, Boris Fouelifack-Nintidem

, Alice Virginie Tchiaze Ifoue

, Andrea Sarah Kenne Toukem

, Odette Massah Dabole

, Oumarou Abdoul Aziz

, Abraham Tchoubou-Sale

, Sedrick Junior Tsekane

, Daniel Kosini

, Pharaon Auguste Mbianda

, Martin Kenne^*

Published in American Journal of Entomology (Volume 8, Issue 3)

Received: 13 July 2024 Accepted: 5 August 2024 Published: 27 August 2024

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Abstract

Synthetic pesticides present risks of pollution of the environment, humans and livestock and the alternative proposed today is to use botanical extracts in the fields against crop pests. But in North Cameroon, little information exists concerning the effect of these extracts on useful pollinating insects in general and no information exists in particular on foragers of the genus Amegilla Friese, 1897 (Apidae: Apinae: Anthophorini). The frequency and foraging activities of Amegilla, on newly blooming flowers of Vigna unguiculata (L.) Walp., 1843 (Fabales: Fabaceae) were recorded during five consecutive days in 2021 and 2022 planting campaigns. Plants were divided into untreated plots and plots treated using the synthetic insecticide Parastar (l p.c..ha^-1) or 10%, 20% and 30% aqueous leaf extracts of Calotropis procera (Aiton) Aiton, 1811 (Gentianales: Apocynaceae), Eucalyptus camaldulensis Dehnh., 1832 (Myrtales: Myrtaceae) and Tithonia diversifolia (Hemsley) Gray, 1883 (Asterales: Asteraceae) respectively. Among 8,987 insects collected (48.9% in 2021), Amegila calens Le Peletier. 1841 with stockier foragers (2021 campaign: 2.2% of the total collection, entomophily F_{A. calens}=4.5%; 2022 campaign: 0.7%, F_{A. calens}=1.3%; pooled campaigns: 2.9%, F_{A. calens}=2.9%) and Amegilla sp. with slender foragers (2021: 3.8%, F_{Amegilla sp.}=7.7%; 2022: no data) were recorded. Foragers started activity from 6 a.m. and stopped foraging before noon, with a peak of activity in 8 to 9 a.m. time slot for A. calens and 10 to 11 a.m. time slot for Amegilla sp.. During the five consecutive days from the first blooming day of the flowers, 598 visits (89.8% in 2021 and 10.2% in 2022) were recorded with a peak of visits during the 3^rd day and then declined until it stopped during the 5^th day. Treatments including the synthetic insecticide (which was the most repellent to the wild bees), did not significantly reduce the frequency of visits. But 20% aqueous extract of Ca. procera showed a significant increased of the mean duration of visits of the bees, compare to the results recorded in Parastar-treated plots. Therefore, the tested extracts, especially 20% aqueous leaves extract of Ca. procera may be recommended to control field insect pests and for preservation of foraging activities of Amegilla genus.

Published in	American Journal of Entomology (Volume 8, Issue 3)
DOI	10.11648/j.aje.20240803.13
Page(s)	76-101
Creative Commons	This is an Open Access article, distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium or format, provided the original work is properly cited.
Copyright	Copyright © The Author(s), 2024. Published by Science Publishing Group

Keywords

Wild Bees, Vigna unguiculata, Synthetic Insecticide, Leaves Extract, Inhibition Effect, Dang

1. Introduction

Apoids are excellent useful pollinator insects

[1-5]

. Pest insects (case of Hemipteran

[6]

) and phytophagous insects (case of Coleoptera and Lepidoptera larvae) damage organs of wild or cultivated plants. Vigna unguiculata (L.) Walp., 1843 (Fabales: Fabaceae) is a largely cultivated plant species in West and Central Africa

[6-9]

. Several studies on the floricultural entomofauna highlighted the negative effect of pest insects

[2]	Otiobo Atibita, E. N. A., Tchuenguem Fohouo, F.-N., Djieto-Lordon, C. Activité de butinage et de pollinisation de Apis mellifera adansonii Latreille (Hymenoptera: Apidae) sur les fleurs d’Oxalis barrelieri (Oxalidaceae) à Yaoundé (Cameroun). Entomologie Faunistique. 2015, 68, 101-108.
[3]	Taimanga, Tchuenguem Fohouo, F.-N. Pollination efficiency of Apis mellifera Linnaeus 1758 (Hymenoptera: Apidae) on Mimosa pudica Linnaeus 1753 (Fabaceae) inflorescences at Yassa (Douala - Cameroon). Journal of Entomology and Zoology Studies. 2018, 6(5), 2027-2033.
[8]	Mohammadou, M., Adamou, M., Taïmanga, Kosini, D., Kenne, M. Seed Yield Improvement in Vigna unguiculata (L.) (Fabaceae): Efficiency of Pollinators and Impact of Aqueous Leaf Extract of Three Plant Species in North Cameroon. Asian Journal of Crop Science. 2023a, 8(3), 146-172. https://doi.org/10.9734/AJRCS/2023/v8i3176 View Article
[9]	Mohammadou, M., Fouelifack-Nintidem, B., Adamou, M., Taimanga, Kossini, D., Tsekane, S. J., Ngamaleu-Siewe, B., Kenne, E. L., Yomon, A. K., Kenne, M. Diversity and Abundance of Pest Insects Associated with Vigna unguiculata (L.) Walp., 1843 (Fabales: Fabaceae) in Bockle and Dang Localities (North-Cameroon). American Journal of Entomology. 2023b, 7(2), 38-61. https://doi.org/10.11648/j.aje.20230702.12 View Article
[10]	Ngegba, P. M., Cui, G., Khalid, M. Z., Zhong, G. Use of Botanical Pesticides in Agriculture as an Alternative to Synthetic Pesticides. Agriculture. 2022, 12(5), 600. https://doi.org/10.3390/agriculture12050600 View Article
[11]	Nghia, N. T., Srivastava, P. Biodiversity of beneficial insect associated with cowpea at Pantnagar, Uttarakhand, India. OMONRICE. 2015, 20, 73-79.
[12]	Anusha, C., Natikar, P. K., Balikai, R. A. Insect pests of cowpea and their management – A review. Journal of Experimental Zoology, India. 2016, 19(2), 635-642.
[13]	Zaki, A. Y., Aly, A. I. Biodiversity of Spider and Other Arthropods Inhabiting Cowpea under Effect of Fish Culture Water and Nitrogen Fertilization and its effect on Yield and Protein at Fayoum Governorate, Egypt. ACARINES. 2018, 12, 87-98. https://doi.org/10.21608/ajesa.2008.164305 View Article
[14]	Manap, T., Fajri, M. Diversity of Bees and Wasp (Hymenoptera) in Cowpea (Vigna sinensis L.) in Agricultural Area at Martapura District, Banjar Regency, South Kalimantan. Journal of Science and Technology. 2020, 9, 29-33. https://doi.org/10.22487/25411969.2019.v9.i2.15174 View Article
[15]	Apriyani, S., Kurnia, A., Sutriadi, M. T. Diversity of insect on cowpea cropping in rain fed land. IOP Conference Series: Earth and Environmental Science. 2021, 739, 012068. https://doi.org/10.1088/1755-1315/739/1/012068 View Article

[2, 3, 8-15]

. Farmers frequently use approved synthetic insecticides

[16]

or unapproved ones in order to control harmful insects. In Adamaoua Region (Cameroon), the synthetic insecticide Parastar (mixture of 20 g.l^-1 imidacloprid and 20 g.l^-1 lamda-cyhalothrin, l p.c..ha^-1) is frequently used

[8, 9, 17]

. The abusive use of synthetic pesticides leads very often to harmful effects on the health of humans, the environment and on useful insects

[18-21]

. They often cause the emergence of resistant forms of pests, the situation being amplified by the impacts of climate change. The negative consequences linked to the excessive and inappropriate use of synthetic chemicals have led researchers to develop alternative methods, including the search for genetically resistant plant varieties and nowadays, more studies are focused on plant extracts which are less expensive, respectful of the environment, accessible to farmers and have little effect on useful insects

[5, 8, 9, 15, 23]

. In Cameroon as in all poor countries, many market gardeners are dragging their feet by adopting very little use of plant extracts, the majority of them declaring using plant extracts in the event of a lack of money for the purchase of synthetic pesticides. The use of plant extracts is now well documented. Among plants of exotic origin, the literature reports the use of leaves extracts of Eucalyptus camaldulensis Dehnh., 1832 (Myrtales: Myrtaceae) native to Australia and the invasive grass Hyptis suaveolens (L.) Poit., 1806 (Lamiales: Lamiaceae) native to tropical America against insects harmful to the cotton Gossypium hirsutum L., 1753 (Malvales: Malvaceae)

[5]

. Among the local origin plants, the literature reports the use of leaves extracts of Gnidia kaussiana Meisner (Myrtyales: Thymeleaceae) and the domesticated wild basil Ocimum canum Sims, 1824 (Lamiales: Lamiaceae), against the cowpea’s post-harvest pest Callosobruchus maculatus (Fabricius, 1775) (Coleoptera: Chrysomelidae)

[20]

. This is also the case of the use of aqueous leaves extract of the “false kinkeliba” Cassia occidentalis L., 1753 (=Senna occidentalis (L.) Link, 1829) (Fabales: Fabaceae) against pest insects on Gossypium hirsutum

[5]

. In the savannah region of Northern-Cameroon, despite the high floral diversity and the flourishing market gardening activity, there is very little information on the insecticidal potential of native plant extracts against pest insects except works concerning the foraging activity and the effect of plant extracts on Apis mellifera Latreille. 1804 (Hymenoptera: Apidae)

[8, 9, 24]

. The wild bees Amegilla Friese, 1897 (Hymenoptera: Apidae) contains about 260 species including unidentified morphospecies

[25]

. Like other species of the Anthophorini tribe, Amegilla are solitary species, do not produce honey, and most of them nest in dry ground in arid or sub arid biomes, steppes, and deserts, giving their English name "digger bees". They are fast flyers, some taxa being nearly impossible to catch because of their incredible agility. Nothing is known about the insecticidal effect of the local wild plant extracts (easily accessible and able to replace Parastar) on Amegilla foragers

[24]

. It was therefore necessary to carry out studies in Adamaoua (Cameroon) on the effect of the leaves extracts of three plant species proposed as botanical insecticides by Mohammadou et al.

[8, 9]

2. Materials and Methods

2.1. Study Site

The study was set up from June to September 2021 and June to October 2022.

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Figure 1. Location of the study site in Dang. A: Adamaoua Region in Cameroon; B: Dang locality (Ngaoundere III suburb).

Cowpea cultivation plots were conducted at Dang locality (7°25'26.42''N, 13°32'24.46'' E; 1107.40 m) (Figure 1). Dang is located in a 3rd district of Ngaoundere, in the agro-ecological zone of the high Guinean savannahs with bimodal rainfall and a Sudano-Guinean climate type.

2.2. Biological Material

Plants of Vigna unguiculata (L.) Walp., 1843 (Fabales: Fabaceae) were from the “Feekem” variety seeds. They were obtained from the station of the Agricultural Research Institute for Development (IRD, Garoua, North-Cameroon) and sown in Dang in experimental plots. Aqueous leaves extracts of Calotropis procera (Aiton) Aiton, 1811 (Gentianales: Apocynaceae), Eucalyptus camaldulensis Dehnh., 1832 (Myrtales: Myrtaceae), and Tithonia diversifolia (Hemsley) Gray, 1883 (Asterales: Asteraceae), were tested as botanical insecticides proposed by Mohammadou et al.

[8, 9]

. E. camaldulensis and Ti. diversifolia leaves were collected in Dang. Ca. procera leaves were collected in Bockle (North, Cameroon). Bees came naturally from neighboring fallows.

2.3. Experimental Device and Procedure

The study was set up in 1,064 m² area using a completely randomized blocks procedure (3.5×4 m² each, four treatments repeated 4 times). Four plots were untreated. Four plots were treated with the approved synthetic insecticide Parastar (mixture of 20 g.l^-1 of imidacloprid and 20 g.l^-1 of lamda-cyhalothrin, l p.c..ha^-1)

[16]

. Thirty-six plots were treated with 10%, 20%, and 30% aqueous leaves extracts in accordance of the procedure described by Mohammadou et al.

[8, 9]

2.4. Formulation of the Botanical Extracts

The aqueous extracts were formulated based on the procedure described by Sreekanth

[21]

which stipulates that one kilogram of the plant powder may be diluted in one litter of distilled water and homogenized before application. The formulation of the synthetic insecticide was that reported in the leaflet. Chemicals were introduced into a manual sprayer and were applied 4 times from 5 p.m. at 7 days interval as soon as the cowpea flowered

[8, 9]

2.5. Data Collection

Data were collected in the field by direct observation in five consecutive days, from the start of flowering of plants, in six time slots each day: 6 to 7 a.m., 8 to 9 a.m., 10 to 11 a.m., 12 a.m. to 1 p.m., 2 to 3 p.m. and 4 to 5 p.m. as presented in our recent publication

[8, 9]

. For each time slots, collected insects were counted, identified in-situ and captured when possible for the identification confirmation in laboratory. Insects were not marked. Results were expressed in terms of the number of visits. Entomophily of the i^th species F_i=(V_i/V_I)*100 was determined with V_i as the number of visits on flowers and V_I as the number of visits of all recorded floricultural insects

[8, 9]

. Abundances in x time period were recorded following direct observation and abundance per 1,000 flowers A_1,000=(A_x/F_x)*1,000 was determined with F_x as the number of controlled flowers and A_x as the number of the target insect species on 1,000 flowers

[8, 9]

. The duration of visits per flower was the time taken by an individual to collect the floral products

[8, 9]

. Foraging speed V_b was the number of flowers visited in one minute V_b=(F_i/d_i)*60 with F_i as the number of flowers visited in d_i time period

[8, 9]

2.6. Data Analysis

Data were stored in an Excel spreadsheet and analyzed using SigmaStat® Version 2.03 software for Windows

[26]

and StatXact-3 Version 3.1 software for exact non-parametric inferences. Results were given in terms of mean ± standard error (se) for quantitative series and absolute or relative abundances for occurrences. Comparisons were set up at the bilateral significance level α=0.05. Comparison of two mean values was set up using the Student t-test from SigmaStat software when the normality and the equal variance test passed. Otherwise we used the Man-Whitney test or the Wilcoxon paired test from SigmaStat software. The simultaneous comparison of more than two quantitative series was set up using the Analysis of Variance test (ANOVA) from SigmaStat software when the conditions of normality and equality of variances passed, followed by pairwise comparisons using the Student-Newman-Keuls procedure. Otherwise, we used the Kruskall-Wallis test from SigmaStat software followed by Dunn procedure. Comparison of two percentages was made using the Fisher’s exact test and the simultaneous comparison of more than two percentages was set up using the asymptotic chi-square test when relevant or the Fisher-Freeman-Halton test from StatXact software. Pairwise comparison of several independent percentages were carried out when using the Fisher’s exact test from StatXact software. The p-values were determined and significance levels were corrected using the sequential Bonferroni procedure

[27]

3. Results

3.1. Abundance and Entomophily of Foragers

Globally 8,987 insect specimens were collected in both years (48.9% in 2021 and 51.1% in 2022). They belonged to eight species amongst which two morphospecies of Amegilla Friese, 1897 (Hymenoptera: Apidae) were identified. Foragers of Amegilla calens Le Peletier. 1841 were stockier (Figure 2A) (2021: 2.2%, entomophily F_{A. calens}=4.5%, one to seven individuals, 2±0, n=99; 2022: 0.7%, F_{A. calens}=1.3%, one to five individuals, 1±0, n=42; pooled years: 2.9%, F_{A. calens}=2.9%, one to seven individuals, 2±0, n=141). Foragers of Amegilla sp. were slender (Figure 2B) (2021: 3.8%, entomophily F_Amegilla_sp.=7.7%, one to eight individuals, 3±0, n=120; 2022: not recorded). Giving in 2021 6.0% of the pooled species (one to eight individuals, 2±0, n=219), 2.9% of A. calens in pooled years (entomophily of Amegilla F_Amegilla=12.2%, one to seven individuals, 2±0, n=141) and 6.7% pooled species in pooled years (F_Amegilla=6.7%, 2±0, n=261).

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Figure 2. Illustration of Amagilla Friese, 1897 (Hymenoptera: Apidae) recorded in Dang (North-Cameroon). A: top view of an adult of Amegilla calens Le Peletier, 1841 (Hymenoptera: Apidae); B: top view of an adult of Amegilla sp. Friese, 1897 (Hymenoptera: Apidae).

In the pooled years, abundances of Amegilla sp. varied from one to eight individuals (3±0, n=120) and the entomophily was F_Amegilla_sp.=3.8%. Wild bees were abundant in 2021 than 2022 (Fisher’s exact test for percentages: p=6.4 x 10-99; Student test for mean values: t=5.994, df=186, p<0.001). Other recorded insects were the sap-sucking Aphis crassivora Koch, 1854 (Hemiptera: Aphididae) (17.9%), the honey-bee Apis mellifera Linnaeus, 1758 (Hymenoptera: Apidae) (34.9%), Danaus plexipus (Linnaeus, 1758) (Lepidoptera: Nymphalidae) (1.0%), Hypolimnas misippus (Linnaeus, 1764) (Lepidoptera: Nymphalidae) (0.8%), the big green grasshopper Tettigonia viridissima (Linnaeus, 1758) (Orthoptera: Tettigoniidae) (2.7%), and Xylocopa olivacea (Fabricius 1778) (Hymenoptera: Apidae) (5.6%).

3.2. Foraging Rhythm of Activity

In the pooled species, foragers began activity around 6 a.m. and stopped it before noon, with a peak of activity between 8 and 9 a.m. (Figure 3A). A. calens showed a daily activity rhythm similar to the pooled species while in Amegilla sp., the peak of activity was noted in 10 to 11 a.m. time slot (Figure 3B). Occurrences of Amegilla sp. recorded in the 6 to 7 a.m. time slot was low in 2021 than 2022 (Fisher-Freeman-Halton test: df=2; p=6.7x10^-5) and it was the same in the 8 to 9 a.m. time slot (Fisher-Freeman-Halton test: df=2; p=1.4x10^-4). The difference was not significant in the 10 to 11 a.m. time slot (Fisher-Freeman-Halton test: df=2; p=0.980) (Figure 3B).

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Figure 3. Daily activity rhythm of Amegilla on cowpea flowers at Dang (Adamaoua Region, North-Cameroon) in 2021 and 2022. A: overall daily activity rhythm of the pooled species showing the peak of activity in 8-9 a.m. time slot; B: daily activity rhythm of Amegilla calens and Amegilla sp. foragers during each campaign.

3.3. Abundance on 1,000 Blooming Flowers

A total of 1,007 essays were set up (402 A. calens in 2021, 252 Amegilla sp. in 2021; 654 pooled species in 2021, 353 A. calens in 2022, and 755 A. calens in pooled years). The number of foragers recorded in one minute A₁ varied from one to nine (A. calens in 2021: 2±0; Amegilla sp. in 2021: 4±0; pooled species in 2021: A₁=3±0; A. calens in 2022: A₁=3±0; pooled species and years: A₁=3±0). Between species in 2021 A₁ mean index was higher in Amegilla sp. than A. calens (Student test: t=1.670, df=652, p<0.001). The number of flowers visited in one minute F₁ varied from five to 689 (A. calens in 2021: five to 689, F₁=178±8; Amegilla sp. in 2021: 24 to 689, F₁=328±13; pooled species in 2021; F₁=236±8; A. calens in 2022: F₁=244±10; pooled species and years: F₁=239±6). Between the two species in 2021 F₁ was high in Amegilla sp. than A. calens (Student test: t=10.216, df=652, p<0.001). The abundance per 1,000 flowers A_1,000 varied from one to 800 (A. calens in 2021: two to 400, A_1,000=18±1; Amegilla sp. in 2021: one to 179, A_1,000=20±2; pooled species in 2021: one to 400 and A_1,000=19±1, A. calens in 2022: one to 800 and A_1,000=29±5; pooled species in pooled years: A_1,000=22±2). Between the two species in 2021 the mean value of A_1,000 was not significant (Student test: t=0.968, df=652, p=0.333). Making A₁=2±0, F₁=209±7, A_1,000=23±2 for A. calens in the pooled years, A₁=3±2, F₁=239±6 and A_1,000=22±2 for the pooled species in the pooled years, A₁ values were in average in 2021, significantly low in A. calens, high in Amegilla sp. while in 2022 they were intermediate between the two extremes in A. calens (ANOVA: F_{(2; 1,004)}=6.381, p<0.001; Student-Newman-Keul test: A. calens in 2021 vs. Amegilla sp. in 2021: p=2x10^-5; A. calens in 2021 vs. A. calens in 2022: p=1x10^-5; Amegilla sp. in 2021 vs. A. calens in 2022: p=1x10^-5). Similar results were noted in F₁ (F_{(2; 1,004)}=4.950, p<0.001; A. calens in 2021 vs. Amegilla sp. in 2021: p=2x10^-5; A. calens in 2021 vs. A. calens in 2022: p=1x10^-5; Amegilla sp. in 2021 vs. A. calens in 2022: p<0.001). In 2021, between the two species A_1,000 variation was significant (F_{(2; 1,004)}=4.004, p=0.019; A. calens in 2021 vs. Amegilla sp. in 2021: p=0.651; A. calens in 2021 vs. A. calens in 2022: p=0.018; Amegilla sp. in 2021 vs. A. calens in 2022: p=0.049).

3.4. Foraging Rate in Five Consecutive Days

In five consecutive days, 598 visits were recorded (89.8% in 2021 and 10.2% in 2022). In both years, occurrences increased in the two first days, reaching the peak in the 3^rd day and then declined until it stopped in the 5^th day (Figure 4A). Between the five days, differences in activity were significant in 2021 except between the 1^st and 4^th day (Figure 4A).

In 2022, not significant differences were noted between the 1^st and 2^nd day, the 1^st and 4^th day, the 2^nd and 3^rd or 4^th day, and between the 4^th and 5^th day (Figure 4A). For both years, the differences were significant except between the 1st and the 2^nd or 4^th day (Figure 4A). For A. calens, on each day, foragers were more active in 2021 than 2022 (Figure 4B). In 2021 A. calens foragers showed no significant difference between the 1^st and 4^th day, and between the 2^nd and 3^rd day (Figure 4B).

In 2022, their behavior was similarly to the situation recorded in the pooled years and pooled species (Figure 4A and 4C). Not significant differences were noted between the 1^st and 2^nd or 4^th day, between the 2^nd and 3^rd or 4^th day, between the 4^th and 5^th day. In the pooled years, the difference was not significant between the 1^st and 2^nd or 4^th day (Figure 4B). Amegilla sp., showed in 2021 no significant difference between the 1^st and 2^nd or 4^th day (Figure 4C).

3.5. Foraging Duration and Speed

In the pooled years, collected only nectar from flowers in one to nine seconds (3.8±0.1, n=1,292). The duration was high in A. calens (one to nine seconds; 4.3±0.1, n=931) than Amegilla sp. (one to eight seconds; 2.7±0.1, n=961) (Student test: t=12.671; df=1,290; p<0.001).

In 2021, the duration varied from one to eight seconds (3.1±0.1, n=403). In Amegilla sp. it was 2.7±0.1 (n=361) in 2021, making a global duration of 2.9±0.1 (n=764).

In 2022, the duration noted in A. calens varied from one to nine seconds (5.2±0.1, n=528). It was higher in 2022 than 2021 (Student-Newman-Keuls test: p<0.001). In pooled years, flowers F_i visited in 60 seconds (mean delay: di=16.4±0.5 seconds, n=778) varied from one to three (F_i=1±0, n=778). Foraging speed V_b varied from one to 24 flowers per minute (8±0, n=778). The overall flowers visited by A. calens in three to 60 seconds (d_i=16.2±0.5, n=563) varied from one to three (F_i=1±0, n=563) and the foraging speed V_b varied from one to 24 flowers per minute (V_b=8±0; n=563).

In 2021, A. calens visited in d_i=16.4±0.7 seconds (n=343), one to three flowers (1±0, n=343). The foraging speed varied from one to 24 flowers per minute (V_b=8±0, n=343). Amegilla sp. visited in d_i=17.0±0.9 seconds (n=215) one to three flowers (F_i=1±0, n=215). The foraging speed V_b varied from one to 24 flowers per minute (V_b=8±0, n=215).

In 2022, A. calens visited in three to 60 seconds (d_i=15.8±0.8, n=220) one to three flowers (F_i=1±0, n=220) and the foraging speed varied from one to 24 flowers per minute (V_b=8±0, n=220).

3.6. Effect of the Leaves Extracts

Parastar inhibited the foraging visits in the pooled years (Figure 5A) and in the pooled species in 2021 (Figure 5B) compared to untreated plots. Plant extracts were between the two extremes. Effect of the plant extracts was little accentuated in 2022 (Figure 5C). In plant extracts plots, inhibition was less accentuated than in Parastar plots. The strongest inhibition was in plots treated with 30% Ti diversifolia (Td30) and the lowest inhibition was in plots treated with 30% E. camaldulensis (Ec30). Plots treated with 10% aqueous leaves extract of Ca. procera (Cp10) or 30% aqueous leaves extract of Ca. procera (Cp30) or even 20% aqueous leaves extract of Ti. diversifolia (Td20) showed comparable effects. Between the two years, variations in the occurrences of the pooled bees and of A. calens foragers were significant except in Parastar plots (Figure 5).

In the pooled years and the pooled bees, occurrences in the treated plots were low compared to untreated plots except comparisons to plots treated with 10% aqueous leaves extract of E. camaldulensis (Ec10) or Ec30 plots (Figure 5A; Table 1A upper part matrix). Occurrences in the Parastar plots were low than the records in plots treated with plant extracts (Figure 5A; Table 1A upper part matrix). Cp10 was not different from other treated plots except when compared to Ec30 plots (Figure 5A; Table 1A upper part matrix). Combinations between other treated plots were not significant except between Ec30 and Td30 (Figure 5A; Table 1A upper part matrix).

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Figure 4. Activity rhythm of Amegilla in five consecutive days from the first day of the flower blooming.

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Figure 5. Effect of the chemical treatments on the visiting rate of the cowpea flowers at Dang locality (Adamaoua Region, North-Cameroon) in 2021 and 2022. Parastar: synthetic insecticide (mixture of 20 g.l^-1 of imidacloprid and 20 g.l^-1 of lamda-cyhalothrin, 1 p.c..ha^-1); Cp10, Cp20 and Cp30: 10%, 20% and 30% respectively of aqueous leaves extract of Calotropis procera (Aiton) Aiton, 1811 (Gentianales: Apocynaceae); Ec10, Ec20 and Ec30: 10%, 20% and 30% respectively of Eucalyptus camaldulensis Dehnh., 1832 (Myrtales: Myrtaceae); Td10, Td20 and Td30: 10%, 20% and 30% respectively of the aqueous leaves extract of Tithonia diversifolia (Hemsley) Gray, 1883 (Asterales: Asteraceae).

Table 1. Pairwise comparisons of the occurrences presented in Figure 5.

Unt.: untreated plots; Para.: Parastar-treated plots (Parastar is a mixture of 20 g.l^-1 of imidacloprid and 20 g.l^-1 of lamda-cyhalothrin, l p.c..ha^-1); Cp10, Cp20, Cp30, Ec10, Ec20, Ec30, Td10, Td20 and Td30 are presented in Figure 5; ns: not significant difference; *: significant difference (p-value<0.05 or p-value<α’): α’: Bonferroni corrected significance level.

In 2021, pooled Amegilla showed a significant difference between the untreated and Parastar plots or Td30 plots, unlike other comparisons (Figure 5B; Table 1A lower part matrix). Parastar plots were different from plots treated with extracts (Figure 5B; Table 1A lower part matrix). Between plant extracts plots, differences were not significant except between Ec30 and Td30 (Figure 5B; Table 1A lower part matrix).

In 2022, bees showed significant differences between untreated plots and all treated plots. Comparisons between treated plots were not significant (Figure 5C; Table 1B upper part matrix). A. callens presented significant differences between untreated plots and treated ones, Parastar plots were different from those treated with plant extracts except when compared to Cp10, Td20 or Td30. Between plots differences were not significant (Figure 5D; Table 1B lower part matrix).

In the case of A. calens in 2021, differences were significant between untreated plots and all treated plots (Figure 5E; Table 1C upper part matrix). Parastar plots were different from others except when compared to Cp10 or Td10. Combinations between plant-extracts plots were not significant (Figure 5E; Table 1C upper part matrix). In the case of A. calens in 2022, untreated plots were different from treated plots except when compared to plots treated with concentrations of E. camaldulensis while comparisons between plots treated with plant extracts (Figure 5F; Table 1C lower part matrix). Amegila sp., showed in 2021, no significant difference between untreated plots and treated plots except between Parastar-treated plots or Td30 plots (Figure 5G; Table 1D). Occurrences noted in Parastar plots were different from other treated plots except from Cp10, Cp30 and Td30 plots. Combinations between plant extract plots were not significant except between EC30 and Td30 (Figure 5G; Table 1D).

During the five consecutive days, occurrences of the bees were less than 10.0% of the total collection (Figure 6). Parastar inhibited the visits of foragers (Figure 6A, 6E, 6I, 6M). The pooled occurrences of the two bee species were in each day, high in untreated plots (Figure 6A, 6M) than in Parastar plots (Figure 6A, 6E, 6M), than records in 2021 (Figure 6E) or 2022 (Figure 6I, 6M) except in the 2^nd day in 2021 (Figure 6E) and the 5th day in the pooled years (Figure 6E). Ca. procera extracts inhibited the visits of the bees but less strongly than the Parastar in 2022. Foragers were no longer recorded in Cp10 plots. They were noted in Cp30 plots (Figure 6B, 6F, 6J). A similar effect was noted in plots treated with E. camaldulensis extracts so that in 2022, visits were absent in the 4^th day (Figure 6C, 6G, 6K). A similar situation was noted in 2022 in plots treated with Ti. diversifolia extracts. Visits were not recorded in the 1^st day and the 5^th day in plots treated with 20% or 30% extracts (Figure 6D, 6H, 6L). In each day, comparisons were not significant except the case of Ti. diversifolia extracts in the 3^rd day (Figure 6N). Between the two years, in the 1^st day, the differences in the occurrences were significant except in the untreated plots, Parastar plots, Cp30 (Figure 6B, 6F, 6J, 6O), Ec10 or plots treated with 20% aqueous leaves extract of E. camaldulensis (Ec20) (Figure 6C, 6G, 6K, 6O) and Td30 (Figure 6D, 6H, 6L, 6O). In the 2^nd day, differences were not significant in untreated plots (Figure 6A, 6E, 6I, 6O), in Parastar plots and in Td30 plots (Figure 6D, 6H, 6L, 6O). On the 3^rd day, the not significant difference was noted in Parastar plots (Figure 6). On the 4^th day, not significant differences were noted in untreated plots, in Cp30 plots and Td30 plots respectively (Figure 6D, 6H, 6L, 6O). On the 5^th day, the differences were not significant except in the combined plots (Figure 6).

In the pooled five days, the differences were all significant between the untreated plots and the plots treated with plant extracts (Figure 6). During the five consecutive days, A. calens occurrence was in all plots and for each plant extract, less than 5.0% of the overall collection (Figure 7). Parastar inhibited the occurrence of foragers, the differences in occurrence being significant except in the 5th day in 2021, the 1^st and 4^th day in 2022 (Figure 7A, 7E, 7I). In each day, the effect of the three extract concentrations of each plant was significant in 2021 on the 3^rd day for Ca. procera, and in the overall data for Ti. diversifolia (Figure 7B, 7F, 7J).

In 2022, the significant variation was noted in Ca. procera extract in the 3rd day (Figure 7C, 7G, 7J). Between the two years, the significant variation was noted in the 1^st day for 10% Ti. diversifolia and the pooled plots (Figure 7C, 7G, 7J). In the 2^nd day, the variation was significant in the untreated plots, plots treated with 20% aqueous leaves extract of Ca. procera (Cp20), Cp30 or Ec30 even or Td20 plots and in the pooled plots (Figure 7D, 7H, 7K). On the 3^rd day, the variation was significant only in untreated plots and the pooled plots (Figure 7D, 7H, 7K). In the 4th day, the variation was significant in the plots Td10 and in the pooled plots (Figure 7D, 7H, 7K). On the 5^th day, no variation was significant (Figure 7D, 7H, 7K). The pooled data showed significant variations except in the case of the Parastar plots (Figure 7D, 7H, 7K). In the case of Amegilla sp., during the two years, the occurrences of A. calens were in all plots and each concentration extract, less than 4.0% of the total collection (Figure 8). The inhibition by Parastar was significant except in the 2nd and the 5^th days (Figure 8A, 8E). Ca. procera and E. camaldulensis extracts did not show any significant variation (Figure 8B, 8F). In the case of Ti diversifolia extracts, the inhibition variation of the visitation rate was significant in the 2^nd day (Figure 8D, 8E). The visit duration was high in 2022 (one to 800 seconds, 29±5, n=353) than 2021 (one to 400 seconds, 19±1, n=654) (Table 2). A_1,000 index showed no significant variation (ANOVA test: F_{(10; 643)}=0.864, p=0.567 for the years and the pooled bees; F_{(10; 744)}=0.612, p=0.805 for the pooled years in A. calens (Table 2A); F_{(10; 643)}=0.864, p=0.567 for the pooled Amegilla in 2021 (Table 2B); F_{(10; 391)}=1.249, p=0.258 for A. calens in 2021 (Table 2C); F_{(10; 241)}=1.093, p=0.368 for Amegilla sp. in 2021 (Table 2D); F_{(10; 342)}=0.525, p=0.872 for A. calens in 2022 (Table 2E). Parastar inhibited the visit duration, dropping it from 4±2 seconds (n=158) in untreated plots to 3.3±0.3 seconds (n=77) in Parastar plots. Plots treated with plant extracts presented intermediate values between the extremes. Plant extracts were not different compared to untreated plots. In Amegilla sp., the untreated plots were not different from Parastar-treated plots or those treated with plant extracts.

Table 2. Number of visits of the wild bees on the blooming flowers.

		A₁			F₁			A_1,000=(A₁/F₁)*1000
	n	Min.	Max.	Mean±se	Min.	Max.	Mean±se	Min.	Max.	Mean±se
A. Pooled years and Amegilla species
Untreated	145	1	8	3±0	5	689	222±16	2	800	24±6
Parastar	61	1	7	2±0	5	640	208±22	2	400	25±7
Cp10	109	1	8	3±0	5	689	250±18	1	800	24±7
Cp20	101	1	8	3±0	15	689	256±20	1	179	19±2
Cp30	56	1	8	3±0	15	689	249±28	1	133	21±3
Ec10	125	1	9	3±0	5	650	212±16	2	800	28±7
Ec20	117	1	9	2±0	5	689	218±18	1	800	27±7
Ec30	54	1	7	3±0	25	689	251±29	1	100	20±3
Td10	102	1	8	3±0	24	689	261±20	1	179	17±2
Td20	91	1	8	3±0	24	689	286±23	1	87	17±2
Td30	46	1	8	3±0	24	650	222±30	3	42	17±2
Pooled plots	1007	1	9	3±0	5	689	239±6	1	800	22±2
ANOVA		F_{(10; 996)}=1.013, p=0.430 ns			F_{(10; 996)}=1.463, p=0.148 ns			F_{(10; 996)}=5.238, p=0.874 ns
B. Pooled Amegilla in 2021
Untreated	95	1	8	2±0	15	689	198±18	2	80	17±1
Parastar	37	1	7	2±0	5	630	237±27	2	400	23±11
Cp10	71	1	8	3±0	24	650	238±23	4	179	19±3
Cp20	65	1	7	3±0	15	650	219±24	3	179	21±3
Cp30	36	1	8	3±0	100	689	342±31	1	59	13±2
Ec10	83	1	9	2±0	15	650	211±21	3	179	20±3
Ec20	77	1	9	2±0	15	650	194±21	3	179	22±3
Ec30	35	1	7	3±0	100	689	330±34	1	59	13±2

Table 2. Continued.

		A₁			F₁			A_1,000=(A₁/F₁)*1000
	n	Min.	Max.	Mean±se	Min.	Max.	Mean±se	Min.	Max.	Mean±se
B. Pooled Amegilla in 2021 (Continued)
Td10	65	1	8	3±0	24	650	241±26	6	179	20±3
Td20	60	1	8	3±0	24	650	255±27	3	87	17±2
Td 30	30	1	8	3±0	35	650	276±42	3	40	14±2
Pooled plots	654	1	9	3±0	5	689	236±8	1	400	19±1
ANOVA		F_{(10; 643)}=2.726, p=0.003 *			F_{(10; 643)}=3.008, p=0.001 *			F_{(10; 643)}=0.864, p=0.567 ns
C. Amegilla calens in 2021
Untreated	60	1	6	2±0	15	600	119±15	3	80	21±2
Parastar	20	1	6	2±0	5	630	185±29	2	400	32±19
Cp 10	43	1	6	2±0	48	650	174±23	6	69	16±2
Cp 20	40	1	6	2±0	15	650	168±24	3	69	18±3
Cp 30	22	1	8	4±0	100	689	351±40	2	30	11±1
Ec 10	53	1	6	2±0	15	650	160±22	3	69	19±2
Ec 20	50	1	6	2±0	15	650	155±23	3	69	19±2
Ec 30	22	1	7	3±0	100	650	335±40	4	30	11±1
Td 10	39	1	6	2±0	48	650	160±24	6	69	17±2
Td 20	35	1	6	2±0	48	650	171±27	3	69	16±2
Td 30	18	1	6	2±0	48	650	172±41	3	40	14±2
Pooled plots	402	1	8	2±0	5	689	178±8	2	400	18±1
ANOVA	F_{(10; 391)}=6.464, p<0.001 *				F_{(10; 391)}=6.147, p<0.001 *			F_{(10; 391)}=1.249, p=0.258 ns
D. Amegilla sp. in 2021
Untreated	35	1	8	3±0	100	689	333±32	2	22	10±1
Parastar	17	1	7	3±0	100	630	299±45	2	35	13±3
Cp 10	28	1	8	4±0	24	650	337±42	4	179	24±7
Cp 20	25	1	7	4±0	24	650	302±43	4	179	25±7
Cp 30	14	1	8	3±1	102	689	326±53	1	59	16±6
Ec 10	30	1	9	3±0	28	650	303±38	4	179	22±6
Ec 20	27	1	9	3±0	24	640	267±39	4	179	28±7
Ec 30	13	1	7	3±1	102	689	322±65	1	59	16±5
Td 10	26	1	8	4±0	24	650	362±45	6	179	25±7
Td 20	25	1	8	5±0	24	650	372±41	6	87	19±3
Td 30	12	1	8	5±1	35	650	431±63	6	29	14±2
Pooled plots	252	1	9	4±0	24	689	328±13	1	179	20±2
ANOVA	F_{(10; 241)}=2.680, p=0.004 *				F_{(10; 241)}=0.833, p=0.597 ns			F_{(10; 241)}=1.093, p=0.368 ns
E. Amegilla calens in 2022
Untreated	50	1	8	4±0	5	650	267±28	2	800	37±16
Parastar	24	1	6	2±0	25	640	164±37	2	100	28±5

Table 2. Continued.

		A₁			F₁			A_1,000=(A₁/F₁)*1000
	n	Min.	Max.	Mean±se	Min.	Max.	Mean±se	Min.	Max.	Mean±se
E. Amegilla calens in 2022 (Continued)
Cp 10	38	1	7	2±0	5	689	273±28	1	800	33±21
Cp 20	36	1	8	3±0	29	689	323±36	1	79	15±3
Cp 30	20	1	6	2±0	15	600	83±28	2	133	35±7
Ec 10	42	1	9	3±0	5	630	214±26	2	800	44±19
Ec 20	40	1	8	3±0	5	689	264±31	1	800	36±20
Ec 30	19	1	6	2±0	25	600	105±33	2	100	32±6
Td 10	37	1	7	2±0	100	689	296±31	1	36	11±2
Td 20	31	1	8	3±0	29	689	347±41	1	79	17±4
Td 30	16	1	8	2±1	24	300	121±22	7	42	22±3
Pooled plots	353	1	9	3±0	5	689	244±10	1	800	29±5
ANOVA	F_{(10; 342)}=2.497, p=0.007 *				F_{(10; 342)}=6.020, p<0.001 *			F_{(10; 342)}=0.525, p=0.872 ns

Pairwise comparisons: Student-Newman-Keul test

A₁: pooled Amegilla in 2021:	Untreated vs. Cp30:	p=0.023 *;	Other comparisons were not significant
A₁: A. calens in 2021:	Untreated vs. Cp30:	p=1x10^-5 *;	Cp20 vs. Cp30:	p=4x10^-5 *;	Cp30 vs. Td30:	p=1.6x10^-4 *
	Untreated vs. Ec30:	p=1x10^-5 *	Cp20 vs. Ec30:	p=5.5x10^-4 *;	Ec 30 vs. Ec 10:	p=4.2x10^-4 *
	Parastar vs. Ec30:	p=0.006 *	Cp30 vs. Ec10:	p=4x10^-5 *;	Ec 30 vs. Ec 20:	p=3.6x10^-4 *
	Parastar vs. Cp30:	p=6.5x10^-4 *;	Cp30 vs. Ec20:	p=2x10^-5 *	Ec 30 vs. Td 10:	p=6.8x10^-4 *
	Cp10 vs. Cp30:	p=2.1x10^-4 *;	Cp30 vs. Td10:	p=6x10^-5 *;	Ec 30 vs. Td 20:	p=0.001 *
	Cp10 vs. Ec30:	p=0.001 *	Cp30 vs. Td20:	p=8x10^-5 *;	Ec 30 vs. Td 30:	p=0.002 *
	Other comparisons were not significant
A₁: Amegilla sp. in 2021:	Parastar vs. Td20:	p=0.029 *	Other comparisons were not significant
A₁: A. calens in 2022:	Untreated vs. Cp10:	p=0.045 *;	Untreated vs. Cp30:	p=0.019 *;
	Other comparisons were not significant
F₁: pooled Amegilla in 2021:	Untreated vs. Cp30:	p=0.006 *;	Cp30 vs. Ec10:	p=0.021 *	Ec10 vs. Ec30:	p=0.047 *
	Untreated vs. Ec30:	p=0.016 *	Cp30 vs. Ec20:	p= 0.007 *;	Ec20 vs. Ec30:	p=0.020 *;
	Cp20 vs. Cp30:	p=0.048 *;	Other comparisons were not significant
F₁: A. calens in 2021:	Untreated vs. Cp30:	p=1x10^-5 *;	Cp20 vs. Cp30:	p=1.8x10^-4 *;	Cp30 vs. Td30:	p=0.003 *
	Untreated vs. Ec30:	p=1x10^-5 *	Cp20 vs. Ec30:	p=6.8x10^-4 *;	Ec10 vs. Ec30:	p=2.4x10^-4 *
	Parastar vs. Cp30:	p=0.001 *;	Cp30 vs. Ec10:	p=5x10^-5 *;	Ec20 vs. Ec30:	p=2.1x10^-4 *
	Parastar vs. Ec30:	p=0.002 *	Cp30 vs. Ec20:	p=4x10^-5 *	Ec 30 vs. Td 10:	p=4.7x10^-4 *
	Cp10 vs. Cp30:	p=8x10^-5 *;	Cp30 vs. Td10:	p=1.3x10^-4 *;	Ec 30 vs. Td 20:	p=9.3x10^-4 *
	Cp10 vs. Ec30:	p=2x10^-4 *	Cp30 vs. Td20:	p=2.8x10^-4 *;	Ec 30 vs. Td 30:	p=0.005 *
	Other comparisons were not significant
F₁: A. calens in 2022:	Untreated vs. Cp30:	p=0.015 *;	Cp20 vs. Cp30:	p=1.4x10^-4 *;	Ec10 vs. Td20:	p=0.039 *;
	Untreated vs. Ec30:	p=0.015 *;	Cp20 vs. Ec30:	p=0.001 *;	Ec20 vs. Ec30:	p=0.016 *
	Untreated vs. Td30:	p=0.046 *;	Cp20 vs. Td30:	p=0.006 *;	Ec20 vs. Td30:	p=0.042 *
	Parastar vs. Cp20:	p=0.019 *;	Cp30 vs. Ec20:	p=0.004 *	Ec 30 vs. Td10:	p=0.006 *
	Parastar vs. Td20:	p=0.007 *;	Cp30 vs. Td10:	p=0.001 *;	Ec30 vs. Td20:	p=3.0x10^-4 *
	Cp10 vs. Cp30:	p=0.005 *;	Cp30 vs. Td20:	p=4.0x10^-5 *;	Td20 vs. Td30:	p=0.002 *
	Cp10 vs. Ec30:	p=0.020 *;	Td10 vs. Td30:	p=0.025 *;	Other comparisons not significant

A₁: number of foragers recorded during one minute on the blooming flowers; F₁: number of the blooming flowers visited in one minutes; A₁₀₀₀: visitation rate per 1000 blooming flowers. ns: not significant difference (p≥0.05); * significant difference (p<0.05). Abbreviations Cp10, Cp20, Cp30, Ec10, Ec20, Ec30, Td10, Td20 and Td30 are presented in Figure 5.

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Figure 6. Effect of the chemical treatments during five first consecutive days of flower blooming on the visiting rate of the cowpea flowers at Dang locality (Adamaoua Region, North-Cameroon) during 2021 and 2022 campaigns. ns: not significant difference (p≥0.05); * significant difference (p<0.05). Abbreviations Cp10, Cp20, Cp30, Ec10, Ec20, Ec30, Td10, Td20 and Td30 are presented in Figure 5.

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Figure 7. Effect of the chemical treatments during five first consecutive days of flower blooming on the visiting rate of Amegilla calens at Dang (Adamaoua Region, North-Cameroon) in 2021 and 2022. ns: not significant difference (p≥0.05); * significant difference (p<0.05). Cp10, Cp20, Cp30, Ec10, Ec20, Ec30, Td10, Td20 and Td30 are presented in Figure 5.

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Figure 8. Effect of the chemical treatments during five first consecutive days of flower blooming on the visiting rate of Amegilla sp. on the cowpea flowers at Dang (Adamaoua Region, North-Cameroon) during the 2021 campaign. ns: not significant difference (p≥0.05).

The Parastar plots were different from Cp10 or Cp20 and Td10. Plots Cp10 or Ec10 were different from Td10 or Td30 plots. The pooled species in the pooled years showed visit durations varying from one to nine seconds (3.8±0.1, n=1292). Pairwise comparisons showed a significant difference only between Parastar plots and Cp20, between Cp20 and Ec30, Td10, Td20 unlike other comparisons (Table 3A, 4A upper part matrix). A. calens in the pooled years showed values varying from one to nine seconds (4.3±0.1, n=931) and a significant difference was noted only between Parastar plots and Cp20, between Cp20 and Ec30 or Td10 (Table 3B, 4A lower part matrix). A. calens in 2021 showed visit durations varying from one to eight seconds (3.06±0.08, n=403) and pairwise comparisons between the untreated plots and those treated, the differences were not significant except when compared to Parastar plots (Table 3C, 4B upper part matrix). Between Parastar plots and treated plots differences were significant except comparisons to Ec20 and Td20 plots (Table 3C, 4B upper part matrix). The Cp10 plots were different only from the Td10 plots (Table 3C, 4B upper part matrix). Cp20 plots were different from Ec20, Td10 and Td20 (Table 3C, 4B upper part matrix). Other comparisons were non-significant (Table 3C, 4B upper matrix). Amegilla sp. in 2021 showed visit durations varying from one to eight seconds (2.66±0.08, n=361). Between the untreated plots and treated ones, the differences were not significant except when compared to Parastar plots (Table 3D, 4B lower part matrix).

In 2022, A. calens showed not significant between plots variation (Table 3E), contrary when compare Parastar plots to Cp20, Cp20 and Ec30 (Table 4C upper part matrix). The difference was significant between Parastar plots and Cp10 or Cp20 or Ec10, between Cp20 and Ec30, Td10 or Td20 (Table 4C lower part matrix). Parastar inhibited the speed from 11±1 flowers per minute (n=115) in untreated plots to 6±1 flowers per minute (n=43) in Parastar plots (Table 5A, 6A upper part matrix). Plots treated with plant extracts were intermediate between the two extremes. Cp20 and Td30 were not different from untreated plots. Parastar plots and Cp10 showed a speed inhibition different from Ti. diversifolia plots. Cp20 or Cp30 presented a foraging speed reduction different from plots treated with E. camaldulensis extracts or Td10. Plots treated with E. camaldulensis extracts showed a significant difference compared to Ti. diversifolia plots. The reduction of the speed in Td10 was different from Td20 or Td30 plots. A. calens in the pooled years showed a not significant difference between Untreated plots and Cp20 or Cp30, Td20 or Td30 (Table 4B, 5A lower part matrix). Not significant differences were noted between Parastar plots and Cp10, Ec10, Ec20 or Ec30. Cp10 plots were different from Cp20 or Cp30, and from Ti diversifolia treated plots. Effect of E. camaldulensis was significant compared to Cp20 or Cp30. Td10 were different from Cp30 and concentrations of E. camaldulensis. Td20 showed a foraging speed different from E. camaldulensis extracts plots. Td30 plots presented a foraging speed different from E. camaldulensis plots or Td10.

Table 3. Mean duration of the visits (in seconds) of the wild bees on the blooming cowpea flowers.

	A. Pooled species in the pooled years				B. Amegilla calens in the pooled years				C. A. calens in 2021
Plots	n	Min.	Max.	Mean±se	n	Min.	Max.	Mean±se	n	Min.	Max.	Mean±se
Unt.	158	1.0	9.0	4.0±0.2	109	1.0	9.0	4.5±0.2	44	1.0	8.0	3.1±0.3
Para.	77	1.0	9.0	3.3±0.3	67	1.0	9.0	3.6±0.3	24	1.0	3.0	1.5±0.1
Cp10	132	1.0	9.0	4.1±0.2	96	1.0	9.0	4.4±0.2	44	2.0	8.0	3.6±0.2
Cp20	137	1.0	9.0	4.5±0.2	96	1.0	9.0	5.1±0.2	41	1.0	6.0	3.8±0.2
Cp30	90	1.0	9.0	3.8±0.2	67	1.0	9.0	4.2±0.3	35	2.0	7.0	3.5±0.3
Ec10	142	1.0	9.0	4.1±0.2	100	1.0	9.0	4.5±0.2	43	1.0	6.0	3.3±0.3
Ec20	144	1.0	9.0	3.7±0.2	98	1.0	9.0	4.4±0.3	40	1.0	7.0	2.5±0.3
Ec30	102	1.0	8.0	3.4±0.2	74	1.0	8.0	3.9±0.2	34	1.0	7.0	3.0±0.3
Td10	105	1.0	9.0	3.4±0.2	75	1.0	9.0	4.0±0.3	30	1.0	7.0	2.5±0.3
Td20	133	1.0	9.0	3.6±0.2	93	1.0	9.0	4.1±0.2	41	1.0	5.0	2.5±0.2
Td30	72	1.0	8.0	3.7±0.3	56	1.0	8.0	4.3±0.3	27	2.0	8.0	3.5±0.3
Pooled plots	1,292	1.0	9.0	3.8±0.1	931	1.0	9.0	4.30±0.07	403	1.0	8.0	3.06±0.08
ANOVA	F_{(10; 1281)}=3.043, p=8x10^-5 *				F_{(10; 920)}=2.534, p=0.005 *				F_{(10; 392)}=5.708, p<0.001 *
Unt. vs. Para	Student test: t=2.326, df=233, p=0.021*				Student test: t=2.731, df=174, p=0.007 *				Student test: t=4.205, df=66, p=8.0x10^-5 *
	D. Amegilla sp. in 2021						E. A. calens in 2022
Plots	n		Min.		Max.		Mean±se		n		Min.		Max.	Mean±se
Unt.	49		1.0		8.0		2.8±0.2		65		1.0		9.0	5.5±0.3
Para.	10		1.0		2.0		1.3±0.2		43		2.0		9.0	4.7±0.3
Cp10	36		2.0		8.0		3.4±0.3		52		1.0		9.0	5.0±0.3
Cp20	41		1.0		6.0		3.1±0.2		55		2.0		9.0	6.0±0.2
Cp30	23		2.0		7.0		2.7±0.3		32		1.0		9.0	5.0±0.4
Ec10	42		1.0		6.0		3.2±0.3		57		2.0		9.0	5.3±0.2

Table 3. Continued.

	D. Amegilla sp. in 2021				E. A. calens in 2022
Plots	n	Min.	Max.	Mean±se	n	Min.	Max.	Mean±se
Ec20	46	1.0	7.0	2.4±0.2	58	1.0	9.0	5.6±0.3
Ec30	28	1.0	7.0	2.3±0.3	40	1.0	8.0	4.6±0.4
Td10	30	1.0	5.0	2.1±0.2	45	1.0	9.0	4.9±0.3
Td20	40	1.0	5.0	2.4±0.2	52	1.0	9.0	5.3±0.3
Td30	16	1.0	4.0	1.8±0.2	29	1.0	8.0	5.0±0.4
Pooled plots	361	1.0	8.0	2.66±0.08	528	1.0	9.0	5.2±0.1
ANOVA	F_{(10; 350)}=3.956, p=4x10^-5 *				F_{(10; 517)}=1.786, p=0.060 ns
Unt. vs. Para.	Student test: t=2.856, df=57, p=0.006 *				Student test: t=1.882, df=106, p=0.063 ns

Unt: Untreated; ns: not significant (p≥0.05); * significant (p<0.05). Cp10, Cp20, Cp30, Ec10, Ec20, Ec30, Td10, Td20 and Td30 are in Figure 5.

Table 4. Student-Newman-Keul pairwise multiple comparisons of the mean values presented in Table 3.

			Aqueous leaves extract: p-value
	Unt.	Para	Cp10	Cp20	Cp30	Ec10	Ec20	Ec30	Td10	Td20	Td30
A. Pooled species in the pooled years (upper part matrix); Amegilla calens in the pooled years (lower part matrix)
Unt.			0.899ns	0.249 ns	0.591ns	0.739ns	0.549ns	0.339ns	0.392ns	0.515ns	0.786ns
Parastar			0.184ns	0.006 *	0.630ns	0.180ns	0.667ns	0.867ns	0.615ns	0.736ns	0.745ns
Cp10	0.901ns	0.281ns		0.177 ns	0.806ns	0.913ns	0.609ns	0.279ns	0.309ns	0.461ns	0.806ns
Cp20	0.091ns	0.001 *	0.929ns		0.213ns	0.298ns	0.054ns	0.010 *	0.010 *	0.022 *	0.198ns
Cp30	0.959ns	0.413ns	0.972ns	0.240ns		0.695ns	0.713ns	0.709ns	0.791ns	0.837ns	0.919ns
Ec10	0.791ns	0.234ns	0.866ns	0.135ns	0.976ns		0.535ns	0.264ns	0.299ns	0.431ns	0.760ns
Ec20	0.952ns	0.268ns	0.166ns	0.195ns	0.930ns	0.964ns		0.726ns	0.828ns	0.852ns	0.930ns
Ec30	0.588ns	0.410ns	0.750ns	0.022 *	0.776ns	0.711ns	0.717ns		0.992ns	0.597ns	0.708ns
Td10	0.686ns	0.550ns	0.806ns	0.038 *	0.740ns	0.785ns	0.760ns	0.824ns		0.849ns	0.852ns
Td20	0.815ns	0.453ns	0.890ns	0.061ns	0.693ns	0.884ns	0.838ns	0.806ns	0.694ns		0.722ns
Td30	0.940ns	0.543ns	0.921ns	0.259ns	0.978ns	0.951ns	0.755ns	0.883ns	0.884ns	0.914ns
B. A. calens in 2021 (upper part matrix); Amegilla sp. in 2021 (lower part matrix)
Unt.			0.566ns	0.408ns	0.712ns	0.574ns	0.384ns	0.765ns	0.366ns	0.183ns	0.641ns
Parastar			2x10^-5*	2x10^-5 *	5x10^-5*	1x10^-4*	0.011ns	0.002*	0.043 *	0.050ns	2x10^-4 *
Cp10	0.340ns	0.005 *		0.672ns	0.731ns	0.792ns	0.033ns	0.536ns	0.060ns	0.021 *	0.914ns
Cp20	0.371ns	0.018 *	0.718ns		0.742ns	0.674ns	0.012 *	0.375ns	0.026 *	0.008 *	0.869ns
Cp30	0.748ns	0.167ns	0.448ns	0.553ns		0.858ns	0.116ns	0.702ns	0.155ns	0.074ns	0.935ns
Ec10	0.411ns	0.010 *	0.664ns	0.721ns	0.534ns		0.185ns	0.689ns	0.211ns	0.097ns	0.686ns
Ec20	0.504ns	0.218ns	0.053ns	0.175ns	0.702ns	0.099ns		0.513ns	0.982ns	0.999ns	0.179ns
Ec30	0.558ns	0.273ns	0.079ns	0.225ns	0.761ns	0.138ns	0.767ns		0.417ns	0.176ns	0.679ns
Td10	0.353ns	0.275ns	0.024 *	0.098ns	0.650ns	0.048 *	0.740ns	0.697ns		0.993ns	0.203ns
Td20	0.432ns	0.267ns	0.067ns	0.175ns	0.487ns	0.114ns	0.917ns	0.923ns	0.849ns		0.108ns
Td30	0.223ns	0.392ns	0.019 *	0.066ns	0.450ns	0.036 *	0.536ns	0.567ns	0.486ns	0.632ns

Unt: Untreated; ns: not significant (p≥0.05); * significant (p<0.05). Cp10, Cp20, Cp30, Ec10, Ec20, Ec30, Td10, Td20 and Td30 are presented in Figure 5.

Table 5. Foraging speed (number of the visited flowers per minute) of the wild bees foragers.

		F_i	d_i	V_b		F_i	d_i	V_b
Plots	n	Min.-Max. (Mean±se)	Min.-Max. (Mean±se)	Min.-Max. (Mean±se)	n	Min.-Max. (Mean±se)	Min.-Max. (Mean±se)	Min.-Max. (Mean±se)
	A. Amegilla calens in the pooled years				B. A. calens in 2021
Untreated	83	1-2 (1±0)	5.0-33.0 (9.5±0.7)	2-24 (11±1)	49	1-2 (1±0)	5.0-33.0 (9.2±0.9)	2-24 (11±1)
Parastar	31	1-2 (1±0)	3.0-60.0 (21.1±2.9)	1-20 (6±1)	19	1-2 (1±0)	3.0-60.0 (22.5±4.1)	1-20 (6±1)
Cp 10	61	1-3 (1±0)	3.0-60.0 (21.0±1.8)	1-20 (6±0)	38	1-3 (1±0)	3.0-60.0 (21.7±2.5)	1-20 (6±1)
Cp 20	58	1-2 (1±0)	5.0-25.0 (11.1±0.8)	3-24 (10±1)	37	1-2 (1±0)	5.0-25.0 (11.1±1.0)	3-24 (10±1)
Cp 30	25	1-2 (1±0)	5.0-8.0 (7.0±0.2)	8-24 (13±1)	16	1-2 (1±0)	5.0-8.0 (7.1±0.3)	8-24 (12±1)
Ec 10	73	1-3 (1±0)	3.0-60.0 (23.6±1.9)	1-20 (6±0)	44	1-3 (1±0)	3.0-60.0 (24.2±2.5)	1-20 (6±1)
Ec 20	67	1-2 (1±0)	3.0-60.0 (23.7±1.9)	1-20 (5±0)	41	1-2 (1±0)	3.0-60.0 (23.6±2.6)	1-20 (5±1)
Ec 30	39	1-2 (1±0)	9.0-50.0 (21.5±1.6)	1-13 (5±1)	23	1-2 (1±0)	9.0-50.0 (21.2±2.0)	1-13 (5±1)
Td 10	49	1-2 (1±0)	5.0-33.0 (13.8±1.0)	2-24 (8±1)	28	1-2 (1±0)	5.0-33.0 (13.9±1.3)	2-24 (8±1)
Td 20	50	1-2 (1±0)	5.0-25.0 (10.7±0.8)	3-24 (10±1)	31	1-2 (1±0)	5.0-25.0 (11.7±1.1)	3-24 (9±1)
Td 30	27	1-2 (1±0)	5.0-8.0 (7.3±0.2)	8-24 (12±1)	17	1-2 (1±0)	5.0-8.0 (7.3±0.3	8-24 (12±1)
ANOVA		F_{(10; 552)}=17.939, p<0.001 *				F_{(10; 332)}=10.383, p<0.001 *
	C. Amegilla sp. in 2021				D. A. calens in 2022
Untreated	32	1-2 (1±0)	5.0-33.0 (10.2±1.3)	2-24 (11±1)	34	1-2 (1±0)	5.0-33.0 (9.9±1.3)	2-24 (11±1)
Parastar	12	1-2 (1±0)	3.0-60.0 (25.7±6.2)	1-20 (6±2)	12	1-2 (1±0)	7.0-56.0 (18.9±4.0)	1-9 (6±1)
Cp 10	24	1-3 (1±0)	5.0-60.0 (22.6±3.6)	1-12 (5±1)	23	1-2 (1±0)	5.0-60.0 (19.8±2.7)	1-12 (6±1)
Cp 20	24	1-2 (1±0)	5.0-25.0 (10.3±1.1)	3-24 (10±1)	21	1-2 (1±0)	5.0-25.0 (11.1±1.4)	3-24 (10±1)
Cp 30	9	1-2 (1±0)	5.0-8.0 (7.1±0.4)	8-17 (11±1)	9	1-2 (1±0)	5.0-8.0 (6.9±0.4)	8-24 (13±2)
Ec 10	27	1-3 (2±0)	3.0-56.0 (25.8±3.3)	1-20 (6±1)	29	1-3 (2±0)	3.0-60.0 (22.8±3.1)	1-20 (6±1)
Ec 20	24	1-2 (1±0)	3.0-56.0 (26.0±3.3)	1-20 (5±1)	26	1-2 (1±0)	5.0-60.0 (23.8±2.9)	1-13 (5±1)
Ec 30	15	1-2 (1±0)	10.0-33.0 (20.7±2.0)	2-12 (5±1)	16	1-2 (1±0)	9.0-50.0 (21.9±2.7)	1-13 (5±1)
Td 10	18	1-2 (1±0)	6.0-25.0 (14.2±1.4)	3-15 (7±1)	21	1-2 (1±0)	5.0-33.0 (13.6±1.7)	2-24 (9±1)
Td 20	21	1-2 (1±0)	5.0-25.0 (10.6±1.3)	3-24 (10±1)	19	1-2 (1±0)	5.0-25.0 (9.1±1.1)	4-24 (11±1)
Td 30	9	1-2 (1±0)	6.0-8.0 (7.4±0.2)	8-17 (12±1)	10	1-2 (1±0)	5.0-8.0 (7.3±0.4)	8-24 (12±2)
ANOVA		F(10; 204)=6.181, p<0.001 *				F(10; 209)=7.579, p<0.001 *

Cp10, Cp20, Cp30, Ec10, Ec20, Ec30, Td10, Td20 and Td30 are presented in Figure 5. ns: not significant difference (p≥0.05); * significant (p<0.05). F_i= Number of the visited flowers; d_i=delay in seconds of the control; V_b: Foraging speed (flowers per minute) using the formula V_b=60 (F_i/d_i).

In 2021, A. calens behaved differently (Table 4C, 5B upper matrix). Cp20, Cp30, Td20, or Td30 were not different from untreated plots. The difference was not significant between Parastar plots and Cp10, Ec10, Ec20 or Ec30, Td10 or Td20. Cp10 plots were not different from E. camaldulensis plots or Td10. Cp20 were not different from Cp30 and from all Ti. diversifolia plots. Cp30 plots showed no significant difference compared to plots Td20 or Td30. Ec10, Ec20 or Ec30 were different from Td20 or Td30. Amegilla sp. presented differences in foraging speed (Table 5D, 6B lower matrix). Untreated plots were not different from Cp20 or Cp30 and Ti. diversifolia plots. Parastar plots were not different from plant extracts plots. Cp10 plots were different from Cp20 or Cp30 and Ti. diversifolia.

Table 6. Pairwise comparisons. Compared means are presented in Table 4.

			Aqueous leaves extracts: α’ (p-value)
	Unt.	Para	Cp10	Cp20	Cp30	Ec10	Ec20	Ec30	Td10	Td20	Td30
A. Pooled campaigns: pooled Amegilla (upper part matrix); Pooled campaigns: Amegilla calens (lower part matrix)
Unt.		2x10^-5*	3x10^-5*	0.123ns	0.446ns	2x10^-5*	3x10^-5*	1x10^-5*	3x10^-5*	0.084ns	0.419ns
Parastar	2x10^-5*		0.875ns	5x10^-5*	3x10^-5*	0.695ns	0.848ns	0.893ns	0.036*	7x10^-5*	2x10^-5*
Cp10	3x10^-5*	0.983ns		2x10^-5*	1x10^-5*	0.888ns	0.698ns	0.852ns	0.011*	2x10^-5*	3x10^-5*
Cp20	0.094ns	7x10^-4*	5x10^-5*		0.080ns	<0.001*	2x10^-5*	3x10^-5*	0.011*	0.893ns	0.127ns
Cp30	0.436ns	3x10^-5*	1x10^-5*	0.060ns		3x10^-5*	1x10^-5*	1x10^-5*	1x10^-3*	0.080ns	0.731ns
Ec10	2x10^-5*	0.885ns	0.966ns	2x10^-5*	3x10^-5*		0.848ns	0.905ns	0.007*	2x10^-5*	3x10^-5*
Ec20	3x10^-5*	0.953ns	0.670ns	2x10^-5*	1x10^-5*	0.876ns		0.838ns	0.005*	3x10^-5*	1x10^-5*
Ec30	1x10^-5*	0.966ns	0.832ns	7x10^-5*	1x10^-5*	0.921ns	0.831ns		0.014*	3x10^-5*	1x10^-5*
Td10	0.002*	0.019*	0.014*	0.148ns	0.003*	0.006*	0.005*	0.016*		0.056*	3x10^-4*
Td20	0.106ns	7x10^-4*	4x10^-5*	0.733ns	0.092ns	2x10^-5*	3x10^-5*	6x10^-5*	0.196ns		0.105ns
Td30	0.522ns	3x10^-5*	3x10^-5*	0.142ns	0.617ns	3x10^-5*	1x10^-5*	1x10^-5*	0.010*	0.167ns
B. 2021 campaign: A. calens (upper part matrix) and Amegilla sp. (lower part matrix)
Unt.		2x10^-4*	3x10^-5*	0.079ns	0.698ns	2x10^-5*	3x10^-5*	1x10^-5*	0.014*	0.088ns	0.657ns
Parastar	0.044*		0.958ns	0.032*	9x10^-4*	0.783ns	0.979ns	0.978ns	0.138ns	0.055ns	0.002*
Cp10	3x10^-4*	0.801ns		0.003*	4x10^-5*	0.990ns	0.886ns	0.922ns	0.158ns	0.017*	1x10^-4*
Cp20	0.707ns	0.083ns	0.003*		0.167ns	0.002*	0.002*	0.008*	0.385ns	0.680ns	0.193ns
Cp30	0.773ns	0.164ns	0.025*	0.853ns		5x10^-5*	3x10^-5*	9x10^-5*	0.031*	0.136ns	0.757ns
Ec10	3x10^-4*	0.618ns	0.853ns	0.003*	0.025*		0.986ns	0.978ns	0.082ns	0.008*	7x10^-5*
Ec20	3x10^-4*	0.903ns	0.952ns	0.003*	0.027*	0.967ns		0.791ns	0.161ns	0.013*	6x10^-5*
Ec30	0.004*	0.965ns	0.995ns	0.020*	0.062ns	0.994ns	0.966ns		0.235ns	0.033*	2x10^-4*
Td10	0.017*	0.853ns	0.782ns	0.782ns	0.115ns	0.706ns	0.856ns	0.939ns		0.378ns	0.050ns
Td20	0.789ns	0.092ns	0.009*	0.036*	0.883ns	0.008*	0.011*	0.044*	0.033*		0.182ns
Td30	0.885ns	0.147ns	0.017*	0.891ns	0.883ns	0.018*	0.018*	0.044*	0.105ns	0.894ns

Table 6. Continued.

			Aqueous leaves extracts: α’ (p-value)
	Unt.	Para	Cp10	Cp20	Cp30	Ec10	Ec20	Ec30	Td10	Td20	Td30
C. A. calens in 2022
Unt.		0.006*	2x10^-4*	0.272ns	0.779ns	4x10^-5*	0.006*	5x10^-4*	0.142ns	0.933ns	0.891ns
Parastar			0.944ns	0.108ns	0.014*	0.993ns	0.738ns	0.949ns	0.263ns	0.018*	0.035*
Cp10				0.024*	0.003*	0.963ns	0.874ns	0.972ns	0.089ns	0.002*	0.009*
Cp20					0.461ns	0.009*	0.009*	0.043*	0.478ns	0.552ns	0.612ns
Cp30						0.002*	8x10^-4*	0.003*	0.234ns	0.691ns	0.679ns
Ec10							0.941ns	0.987ns	0.030*	7x10^-4*	0.005*
Ec20								0.997 ns	0.063 ns	3x10^-4 *	0.003 *
Ec30									0.178 ns	0.003 *	0.010 *
Td10										0.308 ns	0.378 ns
Td20											0.719 ns

Unt: Untreated plots; ns: not significant difference (p≥0.05); * significant difference (p<0.05). Cp10, Cp20, Cp30, Ec10, Ec20, Ec30, Td10, Td20 and Td30 are presented in Figure 5. ns: not significant difference (p≥0.05); * significant (p<0.05).

Cp20 were not different from Cp30, Td10 or Td30. Cp30 were different from Ec10 or Ec20 plots. Ec10, Ec20 or Ec30 were different from Td20 or Td30 plots. Td20 were different from Td10. In 2022, the foraging speed variation was significant in A. calens (Table 5D, 6C). Untreated plots were not different from Cp20, Cp30 or Ti. diversifolia plots. Parastar plots were different from Cp30, Td20 or Td30 (Table 5D, 6C). Cp10 was different from Cp20, Cp30 or Ti. diversifolia plots (Table 5D, 6C). Cp20 or Cp30 were different from E. camaldulensis plots (Table 5D, 6C). Ec10 was different from Ti. diversifolia plots. Ec20 was different from Td20 or Td30 (Table 5D, 6C).

4. Discussion

Floricultural insects in Dang showed a significant activity of Amegilla known as sporadic pollinators

[5, 23, 28]

. The occurrence of Amegilla would depend on the variation of air temperature, humidity, light intensity, precipitations, and the wind. According to Wang et al.

[29]

, bee’s activity increases with light (up to 1000 µmol.m-2.s-1), temperature (up to 28˚C), air humidity (up to 40%), and it decreases at high values

[30]

. In fact, environmental factors have direct impact on flowers and on the sugar content of nectar

[30]

. The peak of activities at the 3rd day may probably correspond to the maximum flowering period. According to Manggoel and Uguru

[31]

, 50% of plant's flowers bloom within two to six days. Absence of Amegilla sp. in 2022 and the variation of the peak of activity mean that wild bees responded differently to the environmental change. Amegilla calens (peak of activity between 8 to 9 a.m.) required certainly low air conditions than Amegilla sp. (activity peak between 10 and 11 a.m.). Plant extracts showed a significant negative impact on wild bees. Plant extracts are least toxic to pollinators

[32]

, easily accessible, inexpensive and biodegradable (pers. obs.). Further studies could elucidate the active molecules. It is well known that imidacloprid is toxic to bees

[33]

, affecting insect’s memory

[34]

and decreasing their longevity

[35]

. The increase of the visits duration may increase the plant’s pollination. Amegilla collected nectar, from 6 a.m. until before noon. This would be due to the availability, attractiveness of the floral products, and the scents from flowers

[36]

. A little earlier activity was noted than what reported at Obala (Centre-Cameroon) with a peak of activity between 9 and 10 a.m.

[37]

. The shift may be due to the prevailing climate which is equatorial forest type in Central Region (Cameroon) and Sudano-Guinean in Dang. Abundance per 1,000 flowers highlighted the attractiveness of the nectar in Ec20 or Ca. procera plots. The low abundance of bees in Parastar plots could be due to the repellent effect of the pesticide. Bees stay longer on flowers very rich in products than on flowers very poor in products. Foraging visit varied according to the treatment type, proving the differential effect of tested pesticides. The variations in the foraging speed could be due to the accessibility, availability of products, distance between flowers and the influence of the plant extracts. Among the approved pesticides

[16]

, Parastar induces changes in reproductive parameters and testicular oxidative stress biomarkers in Wistar male rats

[17]

. Moreover, imidacloprid and lamda-cyhalothrin present a high persistence in the environment. The chronic contact contaminates pollen and nectar and indirectly affect bees

[38-41]

. Imidacloprid (neonicotinoid pesticide) present a long half-life in soils (32 days in sandy loam soils, 38 days in loamy sand soils, 43 days in clay loam soils)

[38-41]

. A long half-life is reported in neurotoxic pyrethroid lamda-cyhalothrin (30 days in average)

[41]

. An abnormal behavior was reported in bees in Taiwan, induced by sub lethal dosage of imidacloprid

[42]

. Five-days control was certainly insufficient (the pesticide not having acted sufficiently) and pesticides were certainly cleaned by rainwater, or insects were reinforced by new ones from neighboring fallows.

5. Conclusions

Untreated plots, Cp20 and Ec20 plots allowed the bees to carry out their activity, unlike Parastar or 30% plant extracts. It would be wise to replace Parastar by 20% plant extracts.

Abbreviations

α	Significance Level
α’	Bonferroni Corrected Significance Level
A. calens	Amegilla calens Le Peletier. 1841
A_1,000	Abundances Per 1,000 Flowers
ANOVA	Analysis of Variance
Ap. mellifera	Apis mellifera Linnaeus, 1758
IRD	Institut de Recherche Agricole Pour le Développement / Agricultural Research Institute for Development
Ca. procera	Calotropis procera (Aiton) Aiton, 1811
Cp10	10% Leaves Extract of Ca. procera
Cp20	20% Extract of Ca. procera
Cp30	30% Extract of Ca. procera
d_i	Delay of the Visits
E. camaldulensis	Eucalyptus camaldulensis Dehnh., 1832
Ec10	10% Extract of E. camaldulensis
Ec20	20% Extract of E. camaldulensis
Ec30	30% Extract of E. camaldulensis
F_i	Visited Flowers
Max	Maximum
Min.	Minimum
MINADER	Ministry of Agriculture and Rural Development (Cameroon)
ns	Not Significant
p-value	Probability Value
Para.	Parastar
se	Standard Error
Ti. diversifolia	Tithonia diversifolia (Hemsley) Gray, 1883
Td10	10% Extract of Ti. diversifolia
Td20	20% Extract of Ti. diversifolia
Td30	30% Extract of Ti. diversifolia
Unt.	Untreated
V. unguiculata	Vigna unguiculata (L.) Walp., 1843
V_b	Foraging Speed

Acknowledgments

The authors acknowledge the Cameroonian Ministry of Higher Education for providing funds through the research support program.

Author Contributions

Taimanga: Conceptualization, Data curation, Investigation, Methodology

Moise Adamou: Conceptualization, Data curation, Investigation, Methodology

Georges Tchindebe: Conceptualization, Data curation, Investigation, Methodology

Moukhtar Mohammadou: Conceptualization, Data curation, Formal Analysis, Investigation, Methodology, Writing – original draft, Writing – review & editing

Ousmana Youssoufa: Formal Analysis, Software, Writing – original draft

Boris Fouelifack-Nintidem: Formal Analysis, Software, Writing – original draft

Alice Virginie Tchiaze Ifoue: Formal Analysis, Software, Writing – original draft

Andrea Sarah Kenne Toukem: Formal Analysis, Software, Writing – original draft

Odette Massah Dabole: Formal Analysis, Software, Writing – original draft

Oumarou Abdoul Aziz: Formal Analysis, Software, Writing – original draft

Abraham Tchoubou-Sale: Formal Analysis, Software, Writing – original draft

Abdel Kayoum Yomon: Formal Analysis, Software, Writing – original draft

Sedrick Junior Tsekane: Formal Analysis, Software, Writing – original draft

Daniel Kosini: Conceptualization, Data curation, Investigation, Methodology

Pharaon Auguste Mbianda: Formal Analysis, Software, Writing – original draft

Martin Kenne: Conceptualization, Data curation, Formal Analysis, Funding acquisition, Project administration, Resources, Software, Supervision, Validation, Writing – original draft, Writing – review & editing

Data Availability Statement

The data is available from the corresponding author upon reasonable request.

Conflicts of Interests

The authors declare no conflicts of interest.

References

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Taimanga, Adamou, M., Tchindebe, G., Mohammadou, M., Youssoufa, O., et al. (2024). Effect of the Botanical Insecticides on Amegilla Friese, 1897 (Hymenoptera: Apidae) Foraging on the Cowpea Flowers in Dang (Adamaoua, North-Cameroon). American Journal of Entomology, 8(3), 76-101. https://doi.org/10.11648/j.aje.20240803.13

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Taimanga; Adamou, M.; Tchindebe, G.; Mohammadou, M.; Youssoufa, O., et al. Effect of the Botanical Insecticides on Amegilla Friese, 1897 (Hymenoptera: Apidae) Foraging on the Cowpea Flowers in Dang (Adamaoua, North-Cameroon). Am. J. Entomol. 2024, 8(3), 76-101. doi: 10.11648/j.aje.20240803.13

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AMA Style

Taimanga, Adamou M, Tchindebe G, Mohammadou M, Youssoufa O, et al. Effect of the Botanical Insecticides on Amegilla Friese, 1897 (Hymenoptera: Apidae) Foraging on the Cowpea Flowers in Dang (Adamaoua, North-Cameroon). Am J Entomol. 2024;8(3):76-101. doi: 10.11648/j.aje.20240803.13

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@article{10.11648/j.aje.20240803.13,
  author = {Taimanga and Moise Adamou and Georges Tchindebe and Moukhtar Mohammadou and Ousmana Youssoufa and Boris Fouelifack-Nintidem and Alice Virginie Tchiaze Ifoue and Andrea Sarah Kenne Toukem and Odette Massah Dabole and Oumarou Abdoul Aziz and Abraham Tchoubou-Sale and Sedrick Junior Tsekane and Daniel Kosini and Pharaon Auguste Mbianda and Martin Kenne},
  title = {Effect of the Botanical Insecticides on Amegilla Friese, 1897 (Hymenoptera: Apidae) Foraging on the Cowpea Flowers in Dang (Adamaoua, North-Cameroon)
},
  journal = {American Journal of Entomology},
  volume = {8},
  number = {3},
  pages = {76-101},
  doi = {10.11648/j.aje.20240803.13},
  url = {https://doi.org/10.11648/j.aje.20240803.13},
  eprint = {https://article.sciencepublishinggroup.com/pdf/10.11648.j.aje.20240803.13},
  abstract = {Synthetic pesticides present risks of pollution of the environment, humans and livestock and the alternative proposed today is to use botanical extracts in the fields against crop pests. But in North Cameroon, little information exists concerning the effect of these extracts on useful pollinating insects in general and no information exists in particular on foragers of the genus Amegilla Friese, 1897 (Apidae: Apinae: Anthophorini). The frequency and foraging activities of Amegilla, on newly blooming flowers of Vigna unguiculata (L.) Walp., 1843 (Fabales: Fabaceae) were recorded during five consecutive days in 2021 and 2022 planting campaigns. Plants were divided into untreated plots and plots treated using the synthetic insecticide Parastar (l p.c..ha-1) or 10%, 20% and 30% aqueous leaf extracts of Calotropis procera (Aiton) Aiton, 1811 (Gentianales: Apocynaceae), Eucalyptus camaldulensis Dehnh., 1832 (Myrtales: Myrtaceae) and Tithonia diversifolia (Hemsley) Gray, 1883 (Asterales: Asteraceae) respectively. Among 8,987 insects collected (48.9% in 2021), Amegila calens Le Peletier. 1841 with stockier foragers (2021 campaign: 2.2% of the total collection, entomophily FA. calens=4.5%; 2022 campaign: 0.7%, FA. calens=1.3%; pooled campaigns: 2.9%, FA. calens=2.9%) and Amegilla sp. with slender foragers (2021: 3.8%, FAmegilla sp.=7.7%; 2022: no data) were recorded. Foragers started activity from 6 a.m. and stopped foraging before noon, with a peak of activity in 8 to 9 a.m. time slot for A. calens and 10 to 11 a.m. time slot for Amegilla sp.. During the five consecutive days from the first blooming day of the flowers, 598 visits (89.8% in 2021 and 10.2% in 2022) were recorded with a peak of visits during the 3rd day and then declined until it stopped during the 5th day. Treatments including the synthetic insecticide (which was the most repellent to the wild bees), did not significantly reduce the frequency of visits. But 20% aqueous extract of Ca. procera showed a significant increased of the mean duration of visits of the bees, compare to the results recorded in Parastar-treated plots. Therefore, the tested extracts, especially 20% aqueous leaves extract of Ca. procera may be recommended to control field insect pests and for preservation of foraging activities of Amegilla genus.
},
 year = {2024}
}

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TY - JOUR
T1 - Effect of the Botanical Insecticides on Amegilla Friese, 1897 (Hymenoptera: Apidae) Foraging on the Cowpea Flowers in Dang (Adamaoua, North-Cameroon)

AU - Taimanga
AU - Moise Adamou
AU - Georges Tchindebe
AU - Moukhtar Mohammadou
AU - Ousmana Youssoufa
AU - Boris Fouelifack-Nintidem
AU - Alice Virginie Tchiaze Ifoue
AU - Andrea Sarah Kenne Toukem
AU - Odette Massah Dabole
AU - Oumarou Abdoul Aziz
AU - Abraham Tchoubou-Sale
AU - Sedrick Junior Tsekane
AU - Daniel Kosini
AU - Pharaon Auguste Mbianda
AU - Martin Kenne
Y1 - 2024/08/27
PY - 2024
N1 - https://doi.org/10.11648/j.aje.20240803.13
DO - 10.11648/j.aje.20240803.13
T2 - American Journal of Entomology
JF - American Journal of Entomology
JO - American Journal of Entomology
SP - 76
EP - 101
PB - Science Publishing Group
SN - 2640-0537
UR - https://doi.org/10.11648/j.aje.20240803.13
AB - Synthetic pesticides present risks of pollution of the environment, humans and livestock and the alternative proposed today is to use botanical extracts in the fields against crop pests. But in North Cameroon, little information exists concerning the effect of these extracts on useful pollinating insects in general and no information exists in particular on foragers of the genus Amegilla Friese, 1897 (Apidae: Apinae: Anthophorini). The frequency and foraging activities of Amegilla, on newly blooming flowers of Vigna unguiculata (L.) Walp., 1843 (Fabales: Fabaceae) were recorded during five consecutive days in 2021 and 2022 planting campaigns. Plants were divided into untreated plots and plots treated using the synthetic insecticide Parastar (l p.c..ha-1) or 10%, 20% and 30% aqueous leaf extracts of Calotropis procera (Aiton) Aiton, 1811 (Gentianales: Apocynaceae), Eucalyptus camaldulensis Dehnh., 1832 (Myrtales: Myrtaceae) and Tithonia diversifolia (Hemsley) Gray, 1883 (Asterales: Asteraceae) respectively. Among 8,987 insects collected (48.9% in 2021), Amegila calens Le Peletier. 1841 with stockier foragers (2021 campaign: 2.2% of the total collection, entomophily FA. calens=4.5%; 2022 campaign: 0.7%, FA. calens=1.3%; pooled campaigns: 2.9%, FA. calens=2.9%) and Amegilla sp. with slender foragers (2021: 3.8%, FAmegilla sp.=7.7%; 2022: no data) were recorded. Foragers started activity from 6 a.m. and stopped foraging before noon, with a peak of activity in 8 to 9 a.m. time slot for A. calens and 10 to 11 a.m. time slot for Amegilla sp.. During the five consecutive days from the first blooming day of the flowers, 598 visits (89.8% in 2021 and 10.2% in 2022) were recorded with a peak of visits during the 3rd day and then declined until it stopped during the 5th day. Treatments including the synthetic insecticide (which was the most repellent to the wild bees), did not significantly reduce the frequency of visits. But 20% aqueous extract of Ca. procera showed a significant increased of the mean duration of visits of the bees, compare to the results recorded in Parastar-treated plots. Therefore, the tested extracts, especially 20% aqueous leaves extract of Ca. procera may be recommended to control field insect pests and for preservation of foraging activities of Amegilla genus.

VL - 8
IS - 3
ER -

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Author Information

Taimanga

Department of Agronomy, Institute of Fisheries and Aquatic Sciences, University of Douala, Douala, Cameroon

Research Fields: Botanical insecticides, Bees, Biological agriculture, Yield agricultural products, Cotton (Gossypium hirsutum), Pollinization

Contact Email

http://orcid.org/0009-0002-3650-2638
Moise Adamou

Laboratory of Applied Zoology, Faculty of Sciences, University of Ngaoundere, Ngaoundere, Cameroon; Faculty of Medicine and Biomedical Sciences of Garoua, University of Garoua, Garoua, Cameroon

Research Fields: Botanical insecticides, Bees, Biological agriculture, Yield agricultural products, Cotton (Gossypium hirsutum), Pollinization

Contact Email

http://orcid.org/0000-0002-4382-4259
Georges Tchindebe

Department of Agronomy, Institute of Fisheries and Aquatic Sciences, University of Douala, Douala, Cameroon

Research Fields: Botanical insecticides, Bees, Biological agriculture, Yield agricultural products, Cotton (Gossypium hirsutum), Pollinization

Contact Email

http://orcid.org/0009-0005-4169-1674
Moukhtar Mohammadou

Laboratory of Biology and Physiology of Animal Organisms, University of Douala, Douala, Cameroon

Research Fields: Botanical insecticides, Bees, Biological agriculture, Yield agricultural products, Cotton (Gossypium hirsutum), Pollinization

Contact Email

http://orcid.org/0009-0008-8986-4150
Ousmana Youssoufa

Laboratory of Applied Zoology, Faculty of Sciences, University of Ngaoundere, Ngaoundere, Cameroon; Laboratory of Biology and Physiology of Animal Organisms, University of Douala, Douala, Cameroon

Research Fields: Botanical insecticides, Bees, Biological agriculture, Yield agricultural products, Cotton (Gossypium hirsutum), Pollinization

Contact Email

http://orcid.org/0009-0008-6109-094X
Boris Fouelifack-Nintidem

Laboratory of Biology and Physiology of Animal Organisms, University of Douala, Douala, Cameroon

Research Fields: Pest control, Entomology, Biology of animal populations, Insects ecology, Applied entomology, Animal ethology

Contact Email

http://orcid.org/0000-0003-1097-3765
Alice Virginie Tchiaze Ifoue

Laboratory of Biology and Physiology of Plant Organisms, University of Douala, Douala, Cameroon

Research Fields: Applied entomology, Insects biology, biostatistics and pollinators, Plant physiology, Soil fertilization

Contact Email

http://orcid.org/0009-0006-0015-380X
Andrea Sarah Kenne Toukem

Laboratory of Biology and Physiology of Animal Organisms, University of Douala, Douala, Cameroon

Research Fields: Toxicology, quality of life, Biostatistics, Animal biology, Public health

Contact Email

http://orcid.org/0009-0008-6261-3984
Odette Massah Dabole

Laboratory of Applied Zoology, Faculty of Sciences, University of Ngaoundere, Ngaoundere, Cameroon; Laboratory of Biology and Physiology of Animal Organisms, University of Douala, Douala, Cameroon

Research Fields: Botanical insecticides, Bees, Biological agriculture, Yield agricultural products, Cotton (Gossypium hirsutum), Pollinization

Contact Email

http://orcid.org/0009-0009-0771-339X
Oumarou Abdoul Aziz

Laboratory of Applied Zoology, Faculty of Sciences, University of Ngaoundere, Ngaoundere, Cameroon; Laboratory of Biology and Physiology of Animal Organisms, University of Douala, Douala, Cameroon

Research Fields: Biopesticides, Insect pest control, Biological agriculture, Bees, Biological agriculture, Pollinization

Contact Email

http://orcid.org/0009-0002-6530-6900
Abraham Tchoubou-Sale

Faculty of Medicine and Biomedical Sciences of Garoua, University of Garoua, Garoua, Cameroon; Laboratory of Biology and Physiology of Animal Organisms, University of Douala, Douala, Cameroon

Research Fields: Botanical insecticides, Bees, Biological agriculture, Yield agricultural products, Cotton (Gossypium hirsutum), Pollinization

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http://orcid.org/0009-0004-3959-0770
Sedrick Junior Tsekane

Laboratory of Biology and Physiology of Animal Organisms, University of Douala, Douala, Cameroon

Research Fields: Applied Zoology, Quality of life and biostatistics, Wildlife Protection, Control of protected areas, Animal Ethology, Animal Ecology

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http://orcid.org/0000-0002-7225-8698
Daniel Kosini

Laboratory of Applied Zoology, Faculty of Sciences, University of Ngaoundere, Ngaoundere, Cameroon; Faculty of Medicine and Biomedical Sciences of Garoua, University of Garoua, Garoua, Cameroon

Research Fields: Conceptualization, Data curation, Investigation, Methodology

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http://orcid.org/0000-0001-9798-0196
Pharaon Auguste Mbianda

Laboratory of Biology and Physiology of Plant Organisms, University of Douala, Douala, Cameroon

Research Fields: Applied entomology, Insects biology, biostatistics and pollinators, Apiculture, Insects-plants interactions, Animal Ethology, Animal Ecology

Contact Email

http://orcid.org/0009-0004-8595-9700
Martin Kenne

Laboratory of Biology and Physiology of Animal Organisms, University of Douala, Douala, Cameroon

Research Fields: Biostatistics, Biology of the Animal Populations, Entomology, Myrmecology, Animal Ethology, Animal Ecology, sociobiology, applied entomology, plant protection, Biological control, pest insects

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http://orcid.org/0000-0002-2104-7073

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APA Style

Taimanga, Adamou, M., Tchindebe, G., Mohammadou, M., Youssoufa, O., et al. (2024). Effect of the Botanical Insecticides on Amegilla Friese, 1897 (Hymenoptera: Apidae) Foraging on the Cowpea Flowers in Dang (Adamaoua, North-Cameroon). American Journal of Entomology, 8(3), 76-101. https://doi.org/10.11648/j.aje.20240803.13

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ACS Style

Taimanga; Adamou, M.; Tchindebe, G.; Mohammadou, M.; Youssoufa, O., et al. Effect of the Botanical Insecticides on Amegilla Friese, 1897 (Hymenoptera: Apidae) Foraging on the Cowpea Flowers in Dang (Adamaoua, North-Cameroon). Am. J. Entomol. 2024, 8(3), 76-101. doi: 10.11648/j.aje.20240803.13

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AMA Style

Taimanga, Adamou M, Tchindebe G, Mohammadou M, Youssoufa O, et al. Effect of the Botanical Insecticides on Amegilla Friese, 1897 (Hymenoptera: Apidae) Foraging on the Cowpea Flowers in Dang (Adamaoua, North-Cameroon). Am J Entomol. 2024;8(3):76-101. doi: 10.11648/j.aje.20240803.13

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@article{10.11648/j.aje.20240803.13,
  author = {Taimanga and Moise Adamou and Georges Tchindebe and Moukhtar Mohammadou and Ousmana Youssoufa and Boris Fouelifack-Nintidem and Alice Virginie Tchiaze Ifoue and Andrea Sarah Kenne Toukem and Odette Massah Dabole and Oumarou Abdoul Aziz and Abraham Tchoubou-Sale and Sedrick Junior Tsekane and Daniel Kosini and Pharaon Auguste Mbianda and Martin Kenne},
  title = {Effect of the Botanical Insecticides on Amegilla Friese, 1897 (Hymenoptera: Apidae) Foraging on the Cowpea Flowers in Dang (Adamaoua, North-Cameroon)
},
  journal = {American Journal of Entomology},
  volume = {8},
  number = {3},
  pages = {76-101},
  doi = {10.11648/j.aje.20240803.13},
  url = {https://doi.org/10.11648/j.aje.20240803.13},
  eprint = {https://article.sciencepublishinggroup.com/pdf/10.11648.j.aje.20240803.13},
  abstract = {Synthetic pesticides present risks of pollution of the environment, humans and livestock and the alternative proposed today is to use botanical extracts in the fields against crop pests. But in North Cameroon, little information exists concerning the effect of these extracts on useful pollinating insects in general and no information exists in particular on foragers of the genus Amegilla Friese, 1897 (Apidae: Apinae: Anthophorini). The frequency and foraging activities of Amegilla, on newly blooming flowers of Vigna unguiculata (L.) Walp., 1843 (Fabales: Fabaceae) were recorded during five consecutive days in 2021 and 2022 planting campaigns. Plants were divided into untreated plots and plots treated using the synthetic insecticide Parastar (l p.c..ha-1) or 10%, 20% and 30% aqueous leaf extracts of Calotropis procera (Aiton) Aiton, 1811 (Gentianales: Apocynaceae), Eucalyptus camaldulensis Dehnh., 1832 (Myrtales: Myrtaceae) and Tithonia diversifolia (Hemsley) Gray, 1883 (Asterales: Asteraceae) respectively. Among 8,987 insects collected (48.9% in 2021), Amegila calens Le Peletier. 1841 with stockier foragers (2021 campaign: 2.2% of the total collection, entomophily FA. calens=4.5%; 2022 campaign: 0.7%, FA. calens=1.3%; pooled campaigns: 2.9%, FA. calens=2.9%) and Amegilla sp. with slender foragers (2021: 3.8%, FAmegilla sp.=7.7%; 2022: no data) were recorded. Foragers started activity from 6 a.m. and stopped foraging before noon, with a peak of activity in 8 to 9 a.m. time slot for A. calens and 10 to 11 a.m. time slot for Amegilla sp.. During the five consecutive days from the first blooming day of the flowers, 598 visits (89.8% in 2021 and 10.2% in 2022) were recorded with a peak of visits during the 3rd day and then declined until it stopped during the 5th day. Treatments including the synthetic insecticide (which was the most repellent to the wild bees), did not significantly reduce the frequency of visits. But 20% aqueous extract of Ca. procera showed a significant increased of the mean duration of visits of the bees, compare to the results recorded in Parastar-treated plots. Therefore, the tested extracts, especially 20% aqueous leaves extract of Ca. procera may be recommended to control field insect pests and for preservation of foraging activities of Amegilla genus.
},
 year = {2024}
}

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TY - JOUR
T1 - Effect of the Botanical Insecticides on Amegilla Friese, 1897 (Hymenoptera: Apidae) Foraging on the Cowpea Flowers in Dang (Adamaoua, North-Cameroon)

VL - 8
IS - 3
ER -

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