Index

ABSTRACT

To evaluate the impact of Apis mellifera (Hymenoptera: Apidae) and other flowering insects on seed production of Zea mays, its foraging and pollinating activities were studied in Yaoundé, during the mild rainy season of 2016 and 2017. Treatments included unlimited plants access by all pollinator insects and bagged plants to avoid all visits. For each year of study, observations were made on 12 plants per treatment. Apis mellifera foraging behavior and effect of pollinator insects in seed yield were evaluated. Results show that this bee foraged pollen on Z. mays panicles during the whole blooming period. The percentage of lines completely filled with seeds, the mean number of seeds per lines and the percentage of normal seeds of unprotected plants were significantly higher than those of plants protected from pollinator insects. Pollinator insects included A. mellifera provoked a significant increment of the percentage of lines completely filled with seeds by 26.80% in 2016, 9.90% in 2017, the mean number of seeds per lines by 31.04% in 2016, 18.96% in 2017 and the percentage of normal seeds by 2.01% in 2016 and 2.53% in 2017. The installation of A. mellifera colonies and nests of pollinator insects close to Z. mays fields is recommended to increase seed yield in the region.

Keywords: Apis mellifera, Zea mays, Panicles, Pollen, Pollination.

DOI: 10.20448/803.3.2.64.71

Citation Dounia; Amada Brahim; Chantal Douka; Stephan Pierre Elono Azang; Clautin Ningatoloum; Roger Belinga Belinga; Francis Gagni Ankemekom; Fomekong Flavie; Joseph Lebel Tamesse; Fernand-Nestor Tchuenguem Fohouo (2018). Foraging Activity of Apis mellifera L. (Hymenoptera: Apidae) on Corn Panicles at Yaoundé, Cameroon. Canadian Journal of Agriculture and Crops, 3(2): 64-71.

Copyright: This work is licensed under a Creative Commons Attribution 3.0 License

Funding : This study received no specific financial support.

Competing Interests: The authors declare that they have no competing interests.

History : Received: 11 September 2018/ Revised: 17 October 2018/ Accepted: 20 November 2018/ Published: 13 December 2018

Publisher: Online Science Publishing

1. INTRODUCTION

In the agroecosystems, insects in general and Apidae in particular have great ecological and economical importance because they have positive influence on pollination [1 ]. Insects’ pollinators can increase fruit yield and best quality of seeds [2 ]. The lack of pollinating insects during flowering time can lead to kidney yields fruits and/or seeds for some crops [3 ]. Maize (Zea mays L.) is originated to Mexico [4 ]. Currently, maize is the most widely grown cereal in the world [5 ]. This poaceae grows well on a wide variety of soils; his biological cycle varies from 90 to 120 days depending on the type of climate [6 ]. The cob is still elongated; covered with modified leaves called spathes and can contain up to 500 seeds [7 ]. Pollination of female flowers is allogamous, but self-pollination is also observed, pollen is produced by male flowers called panicles [6 , 7 ]. All maize in Africa is used for human alimentation; it is also used for animal feed [8 ]. In the industrial sector, starch extracted from dry corn is used for manufacture of alcohol; the oil produced is used for human diet; manufacture of soaps, and production of biofuels [9 ]. In Cameroon the floral entomofauna of Zea mays is not very well studied. The few studies from the literature are that for Tchuenguem, et al. [7 ] which indicate that Halictidae visit the panicles and collected pollen. According to Gallai, et al. [10 ] floral entomofauna of a plant species can vary from one region to another. This work was conducted to study the activity of A. mellifera on Z. mays panicles and determinate assess of pollinator insects on seeds yields of this Poaceae.

2. MATERIALSAND METHODS

2.1. Site and Biological Materials

The studies were conducted from March to June in 2016 and 2017 (mild rainy season) in the fields located at the campus of Higher Teacher’s Training College of University of Yaoundé I (Latitude 10°62' N, Longitude 14°33' E and altitude 756 m) in the Center Region of Cameroon. This region belongs to the tropical rain forest agro-ecological zone [11 ]. The climate is equatorial, guinean-type with four seasons : the peak rainy season (August to November), the peak dry season (November-March), the mild rainy season (March-July) and the mild dry season (July-August); the mean annual temperature is 25°C, while the mean annual relative humidity is 79% [12 ]. The experimental plot was an area of 600 m2. The animal material was represented by insects naturally present in the environment and a colony of Apis mellifera  (Hymenoptera: Apidae) located in the roof of a building at 5 m from the experimental field. Vegetation was represented by wild species and cultivated plants. The plant material was represented by the seeds of Zea mays provided by the Institute of Agricultural Research for Development in Nkolbisson (Yaoundé).

2.2. Planting and Maintenance of Culture

On March 15, 2016 and March 26, 2017, the experimental plot was divided into six sub-plots of (6*6 m2). Seeds were sown on five lines per subplot; each line had six holes and each hole received five seeds. The spacing was 1 m between rows and 1 m on rows. Each hole was 5 cm depth [5 ]. Two weeks after germination (March 30, 2016 and April 8, 2017), the plants were thinned and only two were left per hole. From thinning at the opening of the first panicle (May 12, 2016 and May 21, 2017), weeding was performed manually as necessary to maintain plot weeds-free.

2.3. Study of the Activity of Apis Mellifera on Panicle of Zea Mays

Observations were conducted on individually opened flowers each day, from May 16 to 26 in 2016 and from May 24 to June 4 in 2017 at one hour interval from 7 to 16 h (7-8 h, 9-10 h, 11-12 h,13-14 h, 15-16 h). In a slow walk along all the lines, the identity of all insects that visited panicle of Z. mays was recorded. All insects encountered on panicles were recorded and the cumulated results expressed in number of visits to determine the relative frequency of A. mellifera in the anthophilous entomofauna of Z. mays. Direct observations of the foraging activity of worker bees on panicles were made. The floral products collected by the foragers were recorded for the same dates and time slots as that of the insect counts. The duration of visits [13 ] was timed to the same dates and in four time slots (8-9 h, 10-11 h, 12-13 h, 14-15 h). Abundances (larger numbers of individuals simultaneously active) per panicles and per 1000 panicles (A1000) were recorded on the same dates and times lots as that of there registration of the duration of visits. The first parameter was recorded as a result of direct counts. For the abundance per 1000 panicles, honey bees were counted on aknown number of open panicles; A1000 = [(Ax/Fx)*1000], where Fx  and Ax  are respectively the number of  panicle and the number of individual bees actually counted on Fx [13 ]. During the days of investigation, the temperature and humidity of the study site were recorded every 30 min, from 7 am to 16 pm, using a thermohygrometer installed in the shade.

2.4. Evaluation of the Impact of Pollinator Insects on the yield of Zea Mays

In May 14 and May 22 respectively in 2016 and 2017, 24 plants of Z. mays at the bud stage were labeled.12 of the total plants were allowed for treatment 1 (opened pollination) and 12 others plants belong to treatment 2 (bagged with gauze nets to prevent visitors or external pollinating agents) (figure 1). For each year, three weeks after the withering of the last panicles, the number of seeds formed in the ears of corn for each treatment was counted. The percentage of lines completely filled with seeds, the mean number of seeds per lines and the percentage of normal seeds were then calculated for each treatment. The percentage of lines completely filled with seeds was calculated using the formula: Pri = {[(Pr1 –Pr2) / Pr1]* 100}, where Pr1 and Pr2  are the percentage of line completely filled with seeds in treatment 1 and 2. The percentage of line completely filled with seeds of each treatment (Pr) is Pr = [(P2 / P1)*100], where, P2 is the number of line completely filled by seeds and P1 the number of line initially set. The mean number of seeds per lines and the percentage of normal seeds were then calculated for each treatment.

2.5. Data Analysis

SPSS soft ware and Microsoft Excel were used for three tests: Student's (t) for comparison of means, correlation coefficient (r)  for the study of linear relationship between two variables, Chi-square (χ2) for the comparison of percentages.

3. RESULTS

3.1. Activity of Apis Mellifera on Zea Mays Panicle

3.1.1. Seasonal Frequency of Visits

Amongst the 1076 and 1627 visits of 8 and 11 insects species recorded on Z. mays panicles respectively in 2016 and 2017, A. mellifera was the most represented insect with 892 visits (82.91%) in 2016 and 1025 visits (62.99%) in 2017 (Table 1). The difference between these two percentages is highly significant (χ2 = 124.31; df = 1; p < 0.001).

3.1.2. Floral Substances Harvested

From our field observations, A. mellifera workers were found to collect exclusively pollen on Z. mays panicle (Figure 2).

3.1.3. Abundance ofApis Mellifera Workers

In 2016, the highest mean number of A. mellifera workers simultaneously in activity was four per panicle (n = 30; s = 0.21) and 2832 per 1000 panicles (n = 30; s = 191). In 2017, the corresponding results were three per panicle (n = 30; s = 1.33) and 2120 per 1000 panicles (n = 30; s = 102). The difference  between the mean number of bees per 1000 panicles in 2016 and 2017 was highly significant (t = 68.58; df = 58; p <0.001).

3.1.4. Duration of Visits

In 2016, the mean duration of a visit on Z. mays panicle was 46.23 sec (n = 30; s = 12.36). In 2017, the corresponding figure was 40.50 sec (n = 30; s = 9.86). The difference between the mean duration of the visit in 2016 and 2017 was highly significant (t = 7.55; df = 58; p <0.001).

3.1.5. Daily Rhythm of Visits

Apis mellifera workers were active on Z. mays panicle from 7 am to 16 pm,with a peak of visits between 11-12 am in 2016 and from 7 am to 14 pm with a maximum of visits between 9-10 am in 2017 (Figure 3). Climatic conditions have influenced the activity of A. mellifera workers on Z. mays panicles in field conditions. The correlation was positive and significant between the number of A. mellifera visit son Z. mays panicles and temperature in 2016 (r = 0.88; df = 4; p <0.05) and in 2017 (r = 0.56; df=4; p <0.1). The correlation between the number of visits and the relative humidity of the air was positive and no significant in 2016 (r = 0.25; df=4; p >0.05) and negative and significant 2017 (r = -0.87; df = 4; p <0.05) (figure 3).

3.2. Apicultural Value of Zea Mays

During the mild rainy season, we observed a well elaborated activity of A. mellifera workers on Z. mays panicles. In particular, there was very good pollen collection and workers faithfulness to its panicles. These data allow to place Z. mays in highly polliniferous bee plants.

3.3. Impact of Flower-Feeding Insects in Pollination and Yields of Zea Mays

During pollen harvest, flowering insects of Z. mays were regular shakes panicles releasing the pollen which is then transported by the wind to the female flowers. Thus these insects increased the pollination possibilities of this plant species.Table 2 presents the results on the percentage of lines completely filled with seeds, the mean number of seeds per lines and the percentage of normal seeds in different treatments. From this table, we documented the following:

a- The comparison of the percentage of lines completely filled with seeds showed that the difference was highly significant between treatment 1 (opened plants) and treatment 2 (bagged plants) in the first year (χ2 = 9.84; df = 1; p <0.001) and not significant between these two treatments in the second year (χ2 = 2.09; df = 1; p >0.05). Consequently, in 2016 and 2017, the percentage of lines completely filled with seeds of opened plants was higher than that of bagged plants (χ2 = 9.15; df = 1; p <0.001).

b- The comparison of the mean number of seeds per lines showed that the difference was highly significant between treatments 1 and 2 (t = 169.47; df = 152; p <0.001) in 2016 and in 2017 (t = 91.06; df = 187; p <0.001). Consequently, in 2016 and 2017, a mean number of seeds per lines on ear of the unprotected plants were higher than that of protected plants.

c- The comparison of the percentage of normal seeds showed that the difference was highly significant between opened plants and protected plants on treatments 1 and 2 in the first year (χ2 = 65.41; df = 1; p <0.001) as well as in the second year (χ2 = 99.82; df = 1; p <0.001). Thus, in 2016 and 2017 the percentage of normal seeds in opened plants was higher than that of protected plants in 2016 and in 2017.

The numeric contribution of pollinating insects on the percentage of lines completely filled with seeds, the mean number of seeds per lines and the percentage of normal seeds were respectively 26.80%, 31.04% and 2.01% in 2016. The corresponding figures were 9.70%, 18.96% and 2.53% in 2017. For the two cumulate years, the numeric contributions were 18.25%, 25.00% and 2.27% for the percentage of lines completely filled with seeds, the mean number of seeds per lines and the percentage of normal seeds respectively. The impact of pollinating insects on seeds yields was positive and significant.

4. DISCUSSION

Apis mellifera was the main floral visitor of Z. mays during the observation period. This bee has been reported as the main floral visitor of the panicles of plant in Cameroon [7 ]. Apis mellifera was also shown to be the floral visitors of other plants such as Glycine max in Douala [14 ] Sesamun indicum in Bambui [15 ] Phaseolus vulgaris in Ngaoundéré [16 ] Vitellaria paradoxa in Garoua [17 ] and Gossypium hirsutum in Maroua [18 ]. The peak of the activity of A. mellifera on Z. mays panicles was located between 9 and 12 am, which correlated with the highest availability of pollen on Z. mays panicles. The significant difference between the mean duration of the visit could be attributed to the availability of pollen on the panicles or the variation in the diversity of flowering insects from one year to another. Apis mellifera harvested pollen; this could be attributed to the needs of colonies during the corresponding period or because this Poaceae do not produce nectar. This research indicates that A. mellifera can provide benefits to pollination management of Z. mays. During the collection of pollen on each panicle, A. mellifera foragers were always shakes panicles releasing the pollen which is then transported by the wind to the female flowers. The significant contribution of A. mellifera in seed yield of Z. mays is inagreement in Center Region of Cameroon [7 ]. The weight of A. mellifera played a positive role during pollen collection. Flowering insects shook panicles and could facilitate the liberation of pollen by anthers then transported by the wind from the female flowers for the same plant or the female flowers for another plant of Z. mays [19 ]. The higher production of seeds per lines and that of normal seeds in the treatment with panicles visited by all insects compared to treatment with protected plants howed that A. mellifera and another pollinator insect’s visit were effective in increasing pollination.

5. CONCLUSION

This study reveals that Z. mays is a highly polliniferous bee plant that obtained benefits from the pollination by flowering insects among which A. mellifera is the most important. The comparison of seed sets of protected plants to that of plant visited by all insects under scores the value of these pollinator insects in increasing seed productions as well as seed quality. In the Center Region of Cameroon, the installation of A. mellifera hive close toZ. mays fields is recommended for the increase of theseed yields of this valuable crop.

REFERENCES

[1]          P. Pesson and J. Louveaux, Pollination and plant productions. Paris: INRA, 1984.

[2]          N. Morison, B. E. Vaissière, F. Martin, P. Pécaut, and G. Gambon, "Pollination of artichoke (Cynara scolymus L.) by the domestic honey bee (Apis mellifera L.) in hybrid seed production under grid cover," Apidology, vol. 31, pp. 115-128, 2000.

[3]          F. F.-N. Tchuenguem, D. Djonwangwe, J. Messi, and D. Bruckner, "Foraging and pollination activity of Apis mellifera adansonii Latreille (Hymenoptera: Apidae, Apinae) on the flowers of Helianthus annuus (Asteraceae) in Ngaoundéré (Cameroon)," Cameroon Journal of Experimental Biology, vol. 5, pp. 1-9, 2009.

[4]          G. Valdeyron, Seed production for some field crops: Cereals, grasses and sugar beet. In: Pollination and plant productions, Pesson P. and Louveaux J. (Eds). Paris: INRA, 1984.

[5]          Minader, "Yearbook of agricultural sector statistics, campaigns 2009 & 2010, Directorate of Surveys and Statistics AGRI-STAT Cameroun (Yaoundé)," p. 123, 2012.

[6]          Hoopen and M. Adbou, "Maize production and processing," Pro-Agricultural Collection, Cameroon (Douala), p. 32, 2012.

[7]          F. F.-N. Tchuenguem, J. Messi, and A. Pauly, "The foraging activity of wild Apoids (Hymenoptera Apoidea) on corn flowers in Yaoundé (Cameroon) and reflections on the pollination of tropical grasses," Biotechnology, Agronomy, Society and Environment, Gembloux, vol. 6, pp. 87-98, 2002.

[8]          FAO, State of food insecurity in the world 2009: Economic crises - impacts and lessons learned. Rome, Italy: FAO, 2009.

[9]          C. A. Lamartiniere, "Protection against breast cancer with genistein: A component of soy," The American Journal of Clinical Nutrition, vol. 71, pp. 1705-1707, 2000.Available at: https://doi.org/10.1093/ajcn/71.6.1705s.

[10]        N. Gallai, J.-M. Salles, J. Settele, and B. E. Vaissière, "Economic valuation of the vulnerability of world agriculture confronted with pollinator decline," Ecological Economics, vol. 68, pp. 810-821, 2009.Available at: https://doi.org/10.1016/j.ecolecon.2008.06.014.

[11]        R. Letouzey, Record of the phytogeographical map of Cameroon at 1/500000. Yaoundé: Inst. Map Intern. Vegetation, Toulouse and Institute of Agronomic Research, 1985.

[12]        J. P. Suchet, "The climates of Cameroon," Ph.D. Thesis, University of Bordeaux-France, 1988.

[13]        F. F.-N. Tchuenguem, J. Messi, D. Brückner, B. Bouba, G. Mbofung, and J. H. Hentchoya, "Foraging and pollination behaviour of the African honey bee (Apis mellifera adansonii) on Callistemon rigidus flowers at Ngaoundéré (Cameroon)," Journal of the Cameroon Academy of Sciences, vol. 4, pp. 133-140, 2004.

[14]        Taimanga and F. F.-N. Tchuenguem, "Diversity of flowering insects and its impact on fruit and grain yields of Glycine max (Fabaceae) at Yassa (Douala, Cameroon)," International Journal of Biological and Chemical Sciences, vol. 12, pp. 141-156, 2018.Available at: https://doi.org/10.4314/ijbcs.v12i1.11.

[15]        O. E. N. Atibita, F. F.-N. Tchuenguem, and C. Djieto-Lordon, "Diversidad de la entomofaune floricole de Sesamum indicum (L.) 1753 (Pedaliaceae) son impacto sobre los rendimientos frutílicos y cereales en Bambui (Nord-Ouest, Camerún)," International Journal of Biological and Chemical Sciences, vol. 10, pp. 106-119, 2016.Available at: https://doi.org/10.4314/ijbcs.v10i1.8.

[16]        B. M. T. Kingha, F. F.-N. Tchuenguem, A. Ngakou, and D. Bruuml, "Foraging and pollination activities of Xylocopa olivacea (Hymenoptera, Apidae) on Phaseolus vulgaris (Fabaceae) flowers at Dang (Ngaoundere-Cameroon)," Journal of Agricultural Extension and Rural Development, vol. 4, pp. 330-339, 2012.

[17]        E. Basga, S. T. Fameni, and F. F.-N. Tchuenguem, "Foraging and pollination activity of Xylocopa olivacea (Hymenoptera: Apidae) on Vitellaria paradoxa (Sapotaceae) flowers at Ouro-Gadji (Garoua, Cameroon)," Journal of Entomology and Zoology Studies, vol. 6, pp. 1051-1022, 2018

[18]        Dounia and F. F.-N. Tchuenguem, "Foraging and pollination activity of Apis mellifera adansonii Latreille (Hymenoptera: Apidae) on flowers of Gossypium hirsutum L. (Malvaceae) at Maroua," International Research Journal of Plant Science, vol. 4, pp. 33-44, 2013.

[19]        J. Philippe, Pollination by bees: Laying colonies in the flowering crop to increase yields of crop production: EDISUD the Calade Aix-en-Provence, 1991.

Table-1.Diversity of insects onZea mays panicles in 2016 and 2017, number and percentage of visits of different insects at Yaoundé

Insects  
2016
2017
Total
Order Family
Genus,species,Sub -species
n1
p1%
n2
p2%
n1,2
p1,2%
Coleoptera
(1 sp.)po
5
0.42
6
0.36
11
0.4
Diptera Calliphoridae
(1 sp.)po
0
0
96
5.9
96
3.55
Muscidae
Muscadomesticapo
10
0.93
156
9.58
166
6.14
Hymenoptera Apidae
Apismelliferapo
892
82.91
1025
62.99
1917
70.94
Xylocopaolivaceapo
0
0
103
6.33
103
3.81
 
Amegillasp.po
0
0
53
3.25
53
1.96
Halictidae
Halictussp.po
109
10.13
156
9.58
265
9.81
Eumenidae
Delta sp.po
36
3.34
15
0.92
51
1.88
Vespidae
Synagriscornutapo
0
0
9
0.55
9
0.33
Lepidoptera Acraeidae
Acraeaaceratart
2
0.18
0
0
2
0.08
Nevroptera
(1 sp.) pr
7
0.65
7
0.43
14
0.51
Orthoptera  
(1 sp.)df
15
1.4
1
0.06
16
0.59
Total 12 species
1076
100
1627
100
2703
100

n1 : number of visits on 12 panicles in 10 days. n2 :number of visits on 12 panicles in 10 days. p1 et p2 : percentages of visits. p1=(n1/1076)*100. p2=(n2/1627) *100. n1,2= (n1 + n2). p1,2= [(n1 + n2)/2703]*100. po:visitor collected pollen. df: defoliator. rt: rest. pr: predator. sp.:undetermined species.

Table-2. Percentage of lines completely filled with seeds, mean number of seeds per lines and percentage of normal seeds according to different treatments of Zea mays in 2016 and 2017 at Yaoundé

 
Year
IMP
CCF
% of lines completely filled with seeds
number of seeds per lines
Normal
Total
% Normal
m
s
Seeds
Seeds
seeds
Treatment 1 
2016
12
12
81.11
41.33
3.41
7024
7096
98.98
(opened plants)
Treatment 2 
12
12
59.37
28.5
1.64
5328
5493
96.99
(bagged plants)
Treatment 1 
2017
12
12
85.1
38.66
4.94
7152
7220
(opened plants)
99,05
Treatment 2 
12
12
76.84
31.33
2.08
5484
5680
(bagged plants)
96,54

IMP : isolated maize plant ; CCF : corn cob formed 

Figure-1. Plant of Zea mays isolated from insects

(Dounia, May 30, 2017)

Figure-2. Apis mellifera collecting pollen in a panicle of Zea mays

(Dounia, May 21, 2016)

Figure-3. Mean daily temperature and humidity and mean number of visits of Apis mellifera on Zea mays panicles in 2016 and 2017.

Source of figure 3

7-8. 9-10. 11-12. 13-14. 15-16.

Mean of visits in 2016 0 61,9 88,59 86,59 54,86

Mean of visits in 2017 16.78 58,34 24,87 0 0

Mean of Temperature 19,1 22,4 27,1 21,6 20,1

Mean of hygrometry 70 68 84 86 91