Steeve Ngama, 1) TERRA Teachning and Research Centre, Central African Forests, Department of Biosystems Engineering, Gembloux Agro-Bio Tech, University of Liège, Gembloux, Belgium (e-mail:; 2) Precision Livestock and Nutrition Unit, Gembloux Agro-Bio Tech, University of Liège, Gembloux, Belgium; 3) Agronomic and Forestry Research Institute, National Center for Scientific and Technological Research, Libreville, Gabon (
Lisa Korte, Smithsonian Conservation Biology Institute, Gabon Biodiversity Program, USA; e-mail:
Mireille Johnson, Smithsonian Conservation Biology Institute, Gabon Biodiversity Program, USA; e-mail:
Jérôme Bindelle, Precision Livestock and Nutrition Unit, Gembloux Agro-Bio Tech, University of Liège, Gembloux, Belgium; e-mail:
Auguste Ndoutoume Ndong, Agronomic and Forestry Research Institute, National Center for Scientific and Technological Research, Libreville, Gabon
Cédric Vermeulen, TERRA Teachning and Research Centre, Central African Forests, Department of Biosystems Engineering, Gembloux Agro-Bio Tech, University of Liège, Gembloux, Belgium; e-mail:

Reference to article

Ngama S., Korte L., Johnson M., Bindelle J., Ndoutoume Ndong A., Vermeulen C. 2018. Using camera traps and digital video to investigate the impact of Aethina tumida pest on honey bee (Apis mellifera adansonii) reproduction and ability to keep away elephants (Loxodonta africana cyclotis) in Gamba, Gabon. Nature Conservation Research 3(2): 89–99. DOI: 10.24189/ncr.2018.038

Section Resarch articles

Bees and elephant interactions are the core of a conservation curiosity since it has been demonstrated that bees, one of the smallest domesticated animals, can keep away elephants, the largest terrestrial animals. Yet, insects' parasites can impact the fitness and activity of the bees. Since their activity is critical to the repellent ability against elephants, this study assessed the impact of small hive beetles (Aethina tumida) on bee (Apis mellifera adansonii) reproduction and ability to keep forest elephants (Loxodonta africana cyclotis) away. Because interspecies interactions are not easy to investigate, we have used camera traps and digital video to observe the activity of bees and their interactions with wild forest elephants under varying conditions of hive infestation with the small hive beetle, a common bee pest. Our results show that queen cells are good visual indicators of colony efficiency on keeping away forest elephants. We give evidences that small hive beetles are equivalently present in large and small bee colonies. Yet, results show no worries about the use of bees as elephant deterrents because of parasitism due to small hive beetles. Apis mellifera adansonii bees seem to effectively cope with small hive beetles showing no significant influence on its reproduction and ability to keep elephants away. This study also reports for the first time the presence of Aethina tumida as a constant beekeeping pest that needs to be addressed in Gabon.


Aethina tumida, camera trap, elephants, Gabon, honeybees

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Received: 24.02.2018

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Alonso A., Lee M.E., Campbell P., Pauwels O.S.G., Dallmeier F. (Eds.). 2006. Gamba, Gabon: biodiversity of an equatorial African rainforest. Bulletin of the Biological Society of Washington 12: 1–448.
Amulen D.R., D'Haese M., Ahikiriza E., Agea J.G., Jacobs F.J., de Graaf D.C., Smagghe G., Cross P. 2017. The buzz about bees and poverty alleviation: Identifying drivers and barriers of beekeeping in sub-Saharan Africa. PLoS ONE 12(2): e0172820. DOI: 10.1371/journal.pone.0172820
Blake S., Deem S.L., Mossimbo E., Maisels F., Walsh P. 2009. Forest Elephants: Tree Planters of the Congo. Biotropica 41(4): 459–468. DOI: 10.1111/j.1744-7429.2009.00512.x
Blanc J.J, Barnes R.F.W., Craig G.C., Dublin H.T., Thouless C.R., Douglas-Hamilton I., Hart J.A. 2007. African elephant status report 2007: an update from the African Elephant Database. Gland, Switzerland: IUCN. 275 p. DOI 10.2305/IUCN.CH.2007.SSC-OP.33.en
Bolker B.M., Brooks M.E., Clark C.J., Geange S.W., Poulsen J.R., Stevens M.H.H., White J.-S.S. 2009. Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution 24(3): 127–135. DOI: 10.1016/j.tree.2008.10.008
Burton A.C., Neilson E., Moreira D., Ladle A., Steenweg R., Fisher J.T., Bayne E., Boutin S. 2015. Wildlife camera trapping: a review and recommendations for linking surveys to ecological processes. Journal of Applied Ecology 52(3): 675–685. DOI: 10.1111/1365-2664.12432
Chaiyarat R., Youngpoy N., Prempree P. 2015. Wild Asian elephant Elephas maximus population in Salakpra Wildlife Sanctuary, Thailand. Endangered Species Research 29: 95–102. DOI: 10.3354/esr00706
Cosoroaba I., Chitimia L., Ilie M. 2008. The small hive beetle: A pest of honey bee colonies. Lucrări ştiinłifice medicină veterinară XLI: 437–442.
Cribb B.W., Rice S.J., Leemon D.M. 2013. Aiming for the management of the small hive beetle, Aethina tumida, using relative humidity and diatomaceous earth. Apidologie 44(3): 241–253. DOI: 10.1007/s13592-012-0173-6
Delaplane K.S., van der Steen J., Guzman-Novoa E. 2013. Standard methods for estimating strength parameters of Apis mellifera colonies. Journal of Apicultural Research 52(1): 1–12.
Dosselli R., Grassl J., Carson A., Simmons L.W., Baer B. 2016. Flight behaviour of honey bee (Apis mellifera) workers is altered by initial infections of the fungal parasite Nosema apis. Scientific Reports 6:36649. DOI: 10.1038/srep36649
Fabre Anguilet E., Alabi T., Haubruge É., Nguyen B.K., Bengone Ndong T., Francis F. 2017. Parasitism of Apis mellifera adansonii (Latreille 1804) and Meliponula bocandei (Spinola 1853) by Aethina tumida (Murray 1867): first census in Gabon and impact on domestication. Entomologie Faunistique = Faunistic Entomology 70. Available from:
Grozinger C.M., Richards J., Mattila H.R. 2014. From molecules to societies: mechanisms regulating swarming behavior in honey bees (Apis spp.). Apidologie 45(3): 327–346. DOI: 10.1007/s13592-013-0253-2
Hauser R. 2003. Aethina tumida: la menace se précise. Magazine de l'OVF 6: 21–23.
Hoare R. 2012. Lessons from 15 years of human–elephant conflict mitigation: Management considerations involving biological, physical and governance issues in Africa. Pachyderm 51: 60–74.
Howe E.J., Buckland S.T., Després-Einspenner M.-L., Kühl H.S. 2017. Distance sampling with camera traps. Methods in Ecology and Evolution 8(11): 1558–1565. DOI: 10.1111/2041-210X.12790
Hunt G.J. 2007. Flight and fight: A comparative view of the neurophysiology and genetics of honey bee defensive behavior. Journal of Insect Physiology 53(5): 399–410. DOI: 10.1016/j.jinsphys.2007.01.010
Karidozo M., Osborn F.V. 2005. Can bees deter elephants from raiding crops? An experiment in the communal lands of Zimbabwe. Pachyderm 39: 26–32.
King L.E., Douglas-Hamilton I., Vollrath F. 2011. Beehive fences as effective deterrents for crop-raiding elephants: field trials in northern Kenya. African Journal of Ecology 49(4): 431–439. DOI: 10.1111/j.1365-2028.2011.01275.x
King L.E., Lala F., Nzumu H., Mwambingu E., Douglas-Hamilton I. 2017. Beehive fences as a multidimensional conflict-mitigation tool for farmers coexisting with elephants. Conservation Biology 31(4): 743–752. DOI: 10.1111/cobi.12898
King L.E., Lawrence A., Douglas-Hamilton I., Vollrath F. 2009. Beehive fence deters crop-raiding elephants. African Journal of Ecology 47: 131–137.
Lee M.E., Alonso A., Dallmeier F., Campbell P., Pauwels O.S. 2006. The Gamba complex of protected areas: an illustration of Gabon's biodiversity. Bulletin of the Biological Society of Washington 12: 229–241.
Morgan B.J. 2009. Sacoglottis gabonensis – a keystone fruit for forest elephants in the Réserve de Faune du Petit Loango, Gabon. African Journal of Ecology 47(2): 154–163. DOI: 10.1111/j.1365-2028.2007.00897.x
Nenov D.I., Zlatanova D.P., Stoynov E.H., Peshev H.V., Grozdanov A.P. 2018. Feeding site usage by griffon vultures (Gyps fulvus) in Bulgaria revealed by camera traps. Nature Conservation Research 3(2): 2–12. DOI: 10.24189/ncr.2018.020
Neumann P., Naef J., Crailsheim K., Crewe R.M., Pirk C.W.W. 2015. Hit-and-run trophallaxis of small hive beetles. Ecology and Evolution 5(23): 5478–5486. DOI: 10.1002/ece3.1806
Neumann P., Pettis J.S., Schäfer M.O. 2016. Quo vadis Aethina tumida? Biology and control of small hive beetles. Apidologie 47(3): 427–466. DOI: 10.1007/s13592-016-0426-x
Ngama S., Korte L., Bindelle J., Vermeulen C., Poulsen J.R. 2016. How Bees Deter Elephants: Beehive Trials with Forest Elephants (Loxodonta africana cyclotis) in Gabon. PLoS ONE 11(5): e0155690. DOI: 10.1371/journal.pone.0155690
Ngama S., Korte L., Johnson M., Vermeulen C., Bindelle J. 2018. Camera traps to study the forest elephant's (Loxodonta cyclotis) response to chilli pepper repellent devices in Gamba, Gabon. Nature Conservation Research 3(2): 26–35. DOI: 10.24189/ncr.2018.027
O'Connell A.F., Nichols J.D., Karanth K.U. (Eds.). 2011. Camera Traps in Animal Ecology: Methods and Analyses. Springer Japan. 271 p. DOI: 10.1007/978- 4-431-99495-4
Pearce A.N., Huang Z.Y., Breed M.D. 2001. Juvenile hormone and aggression in honey bees. Journal of Insect Physiology 47(11): 1243–1247. DOI: 10.1016/s0022-1910(01)00109-3
R Core Team. 2017. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. Available from:
Raíces D.S.L., Ferreira P.M., Mello J.H.F., Bergallo H.G. 2017. Smile, you are on camera or in a live trap! The role of mammals in dispersion of jackfruit and native seeds in Ilha Grande State Park, Brazil. Nature Conservation Research 2(4): 78–89. DOI: 10.24189/ncr.2017.045
Seeley T.D., Seeley R.H., Akratanakul P. 1982. Colony Defense Strategies of the Honeybees in Thailand. Ecological Monographs 52(1): 43–63. DOI: 10.2307/2937344
Smit J., Pozo R.A., Cusack J.J., Nowak K., Jones T. 2017. Using camera traps to study the age–sex structure and behaviour of crop-using elephants Loxodonta africana in Udzungwa Mountains National Park, Tanzania. Oryx. P. 1–9. DOI: 10.1017/S0030605317000345
Smith M.L., Koenig P.A., Peters J.M. 2017. The cues of colony size: how honey bees sense that their colony is large enough to begin to invest in reproduction. The Journal of Experimental Biology 220: 1597–1605. DOI: 10.1242/jeb.150342
Smith M.L., Ostwald M.M., Seeley T.D. 2015. Adaptive tuning of an extended phenotype: honeybees seasonally shift their honey storage to optimize male production. Animal Behaviour 103: 29–33. DOI: 10.1016/j.anbehav.2015.01.035
Smith M.L., Ostwald M.M., Seeley T.D. 2016. Honey bee sociometry: tracking honey bee colonies and their nest contents from colony founding until death. Insectes Sociaux 63(4): 553–563. DOI: 10.1007/s00040-016-0499-6
Thibault M., Walsh P.D., Idiata D., Mbina C., Mihindou Y., White L.J.T. 2001. Inventaire de Grands mammifères dans le Complexe d'Aires Protegees de Gamba en 1998 et 1999 (Unpublished report). Libreville: WWF/WCS.
Trolliet F., Huynen M.-C., Vermeulen C., Hambuckers A. 2014. Use of camera traps for wildlife studies. A review. Biotechnology, Agronomy, Society and Environment 18(3): 446–454.
Van Westendorp P. (Ed.). 2006. Beehive construction. British Colombia: Ministry of Agriculture and Land. 15 p.
Zeileis A., Kleiber C., Jackman S. 2008. Regression models for count data in R. Journal of Statistical Software 27: 1–25.
Zlatanova D.P., Popova E.D. 2018. Biodiversity estimates from different camera trap surveys: a case study from Osogovo Mt., Bulgaria. Nature Conservation Research 3(2): 13–25. DOI: 10.24189/ncr.2018.026