Foraging and pollination behaviour of the African honey (Apis mellifera adansonii) on some cultivated and wild in Cameroon

* Fernand - Nestor Tchuenguem Fohouo, University of Ngaoundéré (Cameroon) * Denis Djonwangwe, University of Yaounde I (Cameroon) * Auguste Pharaon Mbianda, University of Ngaoundere (Cameroon) * Jean Messi, University of Yaounde I (Cameroon) * Dorothea Brückner, University of Bremen (Germany) Prof. Dr. TCHUENGUEM FOHOUO Fernand-Nestor

● Entomologist, Beekeeper ● Head of the Beekeeping and Flowering insects-Plants relationships project ● Vice-Dean in charge of Statistics and Student’s Affairs Faculty of Science ● 21 years of research ● 56 Master thesis supervised and 11 under supervision ● 7 PhD Thesis under supervision ● 24 scientific articles and 31 scientific communications. 1. INTRODUCTION

♦ Honey and pollen production depends mainly on the abundance of some species and their attractiveness to honey (Villières, 1987; Segeren et al. 1996).

♦ Thus sustainable beekeeping in a given region needs a detailed knowledge of the bee plants which grow in the environment of the hives (Villières 1987, Bakenga et al. 2000).

♦ Before this study, there was a dearth of literature on the relationship between the honey bee and many plant species in Cameroon. ♦ Nevertheless, in this country, beekeeping need to be developed and the demand for hive products such as honey and pollen is growing.

♦ Highest quantities of honey consumed or marked in Cameroon come from the Adamawa region which has a climate particularly favourable to the proliferation of bees.

♦ This region is equally concerned by the problem of weak beekeeping production. ♦ Main objective: contribute to the knowledge of the relationships between the native honey bees, Apis mellifera adansonii and 37 woody plant species.

♦ Why these plants ? They are among the most representative plant species of the Adamaoua Region of Cameroon. ♦ For each plant species, three specific objectives:

registration of the activity of A. m. adansonii on flowers;

estimation of the apicultural value;

evaluation of the efficacy of A. m. adansonii as pollinator. 2. SITE AND STUDY PERIOD ► Field work : ● Ngaoundéré in the Adamawa Region of Cameroon (Central Africa), during the dry season and the beginning of the rainy season (period of the highest honey production by honey bees in the region ) of 2001-2002 and 2002-2003.

● The region belongs to the high altitude guinean savannah ecological zone. The annual rain fall is about 1500 mm. The mean annual temperature is 22°C. The mean annual relative humidity is 70%.

● Experimental station : Area of 3 km in diameter, centred on a kenyan top – bar hive inhabited by an Apis mellifera adansonii colony.

3. PLANT MATERIAL

► 25 wild species (fruits, fire hood, medicine)  Savannah (23 plants): Annona senegalensis, Bombax pentandrum, Combretum nigricans, Croton macrostachyus, oliveri, Dichrostachys cinerea, Entada africana, Erythrina sigmoidea, Hymenocardia acida, Lannea kerstingii, Lophira lanceolata, Parkia biglobosa, Piliostigma thonningii, Psorospermum febrifugum, Securidaca longepedonculata, Syzygium guineense var. macrocarpum, Tapinanthus sp.a (parasite of S. g. var. macrocarpum), Tapinanthus sp.b (parasite of Piliostigma thonningii), Terminalia macroptera, Trichilia emetica, Vitellaria paradoxa, Vitex madiensis and Ximenia americana.

 Forest gallery (3 plants): Mitragyna ciliata, Syzygium guineense var. guineense and Vitex doniana. ► 12 cultivated (fruits, leaves, ornamentals, hedges): Bixa orellana,Callistemon rigidus, Commiphora kerstingii, Dacryodes edulis, Delonix regia, Eucalyptus camaldulensis, Mangifera indica, Psidium guajava, Persea americana,Terminalia mantaly, Vernonia amygdalina and Voacanga africana.

► Duration of the flowering within each study period 2 months (e.g. Daniellia oliveri and Persea americana) to 6 months (e.g. Callistemon rigidus and Psidium guajava) 4. POPULATIONS Of APIS MELLIFERA ADANSONII STUDIED

► 32 to 67 honey bee colonies located in the observation area.

►Other colonies of Ngaoundere.

► Activity of the honey colonies at the level of thee their hive: for some colonies, between 07.00 and 09.00 h, more than 800 workers entered the hive per minute Uncovered apiary Covered apiary Swarm on a hive Visit of a colonie Traditional hive 5. METHODS

5.1. Study of the foraging activity of A. m. adansonii on flowers of different plant species

► For each plant species which flowers were visited by this bee and for each observation date, the following parameters were registered between 07:00 and 18:00 h:

● floral product harvested during each floral visit (pollen, ); ● abundance of foragers (highest number of workers foraging simultaneously per flower, per flowers of individual plant) ; ● duration of individual flower visit (for pollen, for nectar) ; ● impact of the competitive fauna (disruption of visits) and flora (direct observations , study of the pollen loads of some workers). 5.2. Evaluation of the apicultural value of different plant species

►The apicultural value of each plant studied was evaluated using data on:

● the flowering intensity;

● the attractiveness of A. m. adansonii worker with respect to nectar or pollen. 5.3. Evaluation of the influence of Apis mellifera adansonii on pollination

► Visits during which the honey bee came into contact with the stigma (Jacob-Remacle 1989; Freitas 1997) were counted while the duration of the flower visits were recorded 5.4. Data analyses

Data were subjected to descriptive statistics, Student’s t – test and correlation analysis using Microsoft Excel software. 6. RESULTS AND DISCUSSION

6.1. Apis mellifera adansonii activity on flowers of different plant species

► Floral products harvested, intensity and frequency of collection of different products :

♣ Number of observation days: 24 (Vitex doniana) to 96 (e.g. Voacanga africana)

●Plants visited of pollen only: Bixa orellana, Dicrostachys cinerea and Piliostigma thonningii. ● Plant visited for nectar only: 10 species, e.g. Mytragina ciliata, Parkia biglobosa and Dacryodes edulis;

● Plant sisited nectar and pollen: 24 species, eg. Callistemon rigidus, Vitex madiensis and Daniellia oliveri;

● In general, the intensity of nectar or pollen collection varied with plant species and time;

● Frequency of nectar harvest (compared to the number of observation days): 30.37% (P. guajava) to 100% (19 plants, e.g. Vitellaria paradoxa);

● frequency of pollen harvest: 9.38% (Tapinanthus sp.a) to 100% (5 plants, e.g. Croton macrostachyus). Combretum nigricans (Combretaceae) A. m. adansonii workers harvested nectar on Vernonia amygdalinaflorets .

Vernonia amygdalina (Asteraceae) Persea americana (Lauraceae) ► Density of foragers

●per flower: from 1 (28 species, e.g. Persea americana and Erythrina sigmoidea) to 4 workers (4 species, e.g. Psidium guajava and Bombax pentandrum).

● per flowers of a plant: from 6 (Piliostigma thonningii) to 4200 workers (Bombax pentandrum and Vernonia amygdalina).

● The observed high abundance of foragers per individual plant were reported to be due to the ability of honey bees to recruit a great number of workers for the exploitation of high yield food sources (Frisch 1969, Louveaux 1984, Schneider and Hall 1997). Duration of visits per flower ● the mean duration of a flower visit varied with plant species and for a plant species, with the type of floral product.

● The difference between the mean duration of a flower visit for nectar collection and that for pollen collection was highly significant in 18 plants:

- e.g.1, L. kerstingii, in 2001/2002 (n =54, m=3.63 sec, s = 1.55 for pollen ; n =54, m = 2.54 sec, s = 1.25 for nectar; t = 4.02, P < 0.00001);

- e.g.2 V. amygdalina, in 2002/2003 (n =210, m=1.01 sec, s = 0.12 for pollen ; n =210, m = 1.08 sec, s = 0.27 for nectar; t = 3.43, P < 0.001).

Thus, on a flower of L. kerstingii, A. m. adansonii spent more time for pollen collection than for nectar harvesting, whereas on a flower of V. amygdalina this bee spent more time for nectar collection than for pollen harvesting. ► The duration of visits was partially influenced by the anthophilous fauna via disruptions. Thus for 108 visits registered on L. kerstingii flowers in 2001/2002, 39 were disrupted by A. m. adansonii (21 visits), Meliponula ferruginea (7), Ceratina sp. (5), Camponotus flavomarginatus (3) and Paratrechina longicornis (3).

► These disruptions reduced the duration of certain A. m. adansonii visits. This obliged some workers bees to visit more flowers during a foraging trip, in order to obtain their maximal pollen or nectar loads. Some flowering insects (Bees and Wasps) of Cameroon Influence of neighbouring flora

► During one foraging trip, an individual bee foraging on a given plant species scarcely visited another plant species. ► The analysis of the pollen loads of worker bees shows that, the percentage of the foreign pollen grain varied from 0.13% in Hymenocardia acida and Delonix regia to 8.86% in Ximenia americana.

► This result indicates that A. m. adansonii shows flower constancy (Louveaux 1984, Backhaus 1993, Basualdo et al. 2000) for the flowers of each plant species studied. 6.2. Apicultural value of different plant species

Obtained data allow plant species studied to be classify in seven categories of bee plants:

Categories of bee plants Plant species Nb Examples Wild Cultivated Very highly nectariferous (4) 27 D. oliveri V. africana Highly nectariferous (3) 4 T. macroptera Slightly nectariferous (2) 3 P. febrifugum T. mantaly Very highly polliniferous (4) 7 L. kerstingii B. orellana Highly polliniferous (3) 10 X. americana E. camaldulensis Slightly polliniferous (2) 8 L. lanceolata C. rigidus Very slightly polliniferous (1) 3 P. febrifugum C. kerstingii Months indicated for honey collection in an environment which is rich in ten of the bee plants studied.

Plant species Months December J Februaryanuary March April M ayJune

Vitellaria paradoxa Lophira lanceolata S. g. var. macrocarpum Daniellia oliveri Callistemon rigidus Voacanga africana Parkia biglobosa Ximenia americana Vitex madiensis Croton macrostachyus Honey com 6.3. Impact of Apis mellifera adansonii activity on pollination of the plant species

● During the collection of pollen or nectar on the flowers of each plant, foragers regularly contacted anthers and carried pollen with which they flew frequently from flower to flower. ● For 30 plants, the percentage of the total number visits during which worker bees came into contact with the stigma of the visited flower varied from 12.50% in Bombax pentandrum to 100 % e.g. in Annona senegalensis

● Thus A. m. adansonii workers could induce self- pollination and/ or cross-pollination (geitonogamy or xenogamy). Ximenia americana (Olacaceae) Ximenia americana on a local market Number of flowering insect species, main pollinating insects and contribution of pollinating insects to the yields of four plant species.

Plant species Nb flowering Two major % contribution insect species pollinating of pollinating insects insects to fruit yields

Callistemon rigidus 23 Apis mellifera adansonii 57 (Myrtaceae) Belonogaster juncea

Dacryodes edulis > 57 Meliponula erythra 55 (Burseraceae) Apis mellifera adansonii

Syzygium guineense 93 Apis mellifera adansonii 38 (Myrtaceae) Lasioglossum sp.

Voacanga africana 106 Apis mellifera adansonii 93 (Apocynaceae) Musca domestica 7. CONCLUSION

♣ Based on our results, we recommended : (i) the installation of A. m. adansonii colonies in environments where one or more of the studied plant species occur abundantly;

(ii) the cultivation and/or the protection of each plant species, except Tapinanthus spp., in the surroundings of A. m. adansonii apiaries.

♣Furthermore, insecticide treatments should be avoided during the flowering period of each plant species studied. ♣ If these treatments are necessary, the integrated pest control should be recommended to protect pollinating insects such as A. m. adansonii. Publications

1- TCHUENGUEM FOHOUO (F.-N), DJONWANGWE (D.), MESSI (J.) & BRÜCKNER (D.), 2007.- Exploitation of Entada africana, Eucaalyptus camaldulensis, Psidium guajava and Trichillia emetica flowers by Apis mellifera adansonii at Dang (Ngaoundéré, Cameroon). Cameroon Journal of Experimental biology, 3(2): 50-60.

2- TCHUENGUEM FOHOUO (F.-N), DJONWANGWE (D.) & BRÜCKNER (D.), 2008.- Foraging behaviour of the African honey bee (Apis mellifera adansonii) on Annona senegalensis, Croton macrostachyus, Psorospermum febrifugum and Syzygium guineense var guineense flowers at Ngaoundéré (Cameroon). Pakistan Journal of Biological Sciences. 11(5) : 719-725.

3- TCHUENGUEM FOHOUO (F.-N), DJONWANGWE (D.), MESSI (J.) & BRÜCKNER (D.), 2008.- Exploitation of Dichrostachys cinerea, Vitellaria paradoxa, Persea americana and Securidaca longepedunculata flowers by Apis mellifera adansonii Latreille (Hymenoptera: Apidae) at Dang (Ngaoundéré, Cameroon). International Journal of Tropical Insect Science, 28(4): 225- 233.

NB: four ‘In press’ or ‘submited’ Perspectives on beekeeping and insect pollination :

● construction at the University of Ngaoundere of a reference center for training and research on beekeeping and insect pollination.

● more education of the public on hive products and the impact of bees and other pollinating insects on plant yields.

● more inventory of pollinating insect species.

● production of movies on beekeeping and pollinating insects in Cameroon, to strengthen research and training on these topics. ● optimal exploitation of data from the beekeeping literature.

● development of beekeeping as an answer to the problems of desertification in Cameroon. ACKNOWLEGMENTS

► This study was funded by the International Foundation for Science (IFS ; Stockholm, Sweden) and the United Nation University (UNU ; Tokyo, Japan) via a research grant to TFFN (3181-1). ► The DAAD (German Academic Exchange Programme has awarded a research grant to TFFN (A/08/15704) to strengthen the collaboration among authors.

► We thank A. Pauly for its contribution to the identification of flowering insects and P.M. Mapongmetsem for the identification of plant species.

► Our participation in this APIMONDIA 2009 Congresss is funded by the Bee Unit of the University of Bremen (Germany).