Abdullahi Ahmed Yusuf

Honeybee health in Africa—a review

Honeybee (Apis mellifera L.) pathogens and parasites and the negative effects thereof on honeybee populations remain an issue of public concern and the subject of active research. Africa with its high genetic diversity of honeybee sub-species and large wild population is also exposed to various factors responsible for colony losses in other parts of the world. Apart from the current American foulbrood epidemic in the Western Cape of South Africa, no large-scale colony losses have been reported elsewhere on the continent. We discuss the presence of pathogens, parasites, pests and predators of African honeybees as well as the threats they face in relation to habitat changes arising from the impact of increased human populations. In addition, we discuss current efforts aimed at protecting and promoting the health of African honeybees.

Nestmate recognition and the role of cuticular hydrocarbons in the African termite raiding ant Pachycondyla analis

Cuticular hydrocarbons (CHCs) are used for chemical communication among nestmates in many ant species, and they may play a role in the discrimination of nestmates and non-nestmates. Using the mandible opening response (MOR) bioassay, we tested the response of the African termite raiding ant, Pachycondyla analis, to CHC extracts of nestmates and non-nestmates. The ants were able to distinguish control chemical cues, from nestmate CHCs, and from non-nestmate CHCs, and, based on a CHC recognition threshold, aggression was demonstrated toward non-nestmates. Gas chromatography (GC) and GC-mass spectrometric analyses showed that CHC components of different ant colonies had chain lengths ranging from C8 to C31, comprising mainly n-alkanes, alkenes, and methyl branched alkanes, with the n-alkanes occurring in the same proportions among all colonies. The ants were grouped successfully according to their colonies of origin by using discriminant analysis of CHCs. We demonstrate that nestmate recognition occurs in P. analis, and that some of the cues involved are evidently alkenes and methyl-branched alkanes.

The Only African Wild Tobacco, Nicotiana africana: Alkaloid Content and the Effect of Herbivory

Herbivory in some Nicotiana species is known to induce alkaloid production. This study examined herbivore-induced defenses in the nornicotine-rich African tobacco N. africana, the only Nicotiana species indigenous to Africa. We tested the predictions that: 1) N. africana will have high constitutive levels of leaf, flower and nectar alkaloids; 2) leaf herbivory by the African bollworm Helicoverpa armigera will induce increased alkaloid levels in leaves, flowers and nectar; and 3) increased alkaloid concentrations in herbivore-damaged plants will negatively affect larval growth. We grew N. africana in large pots in a greenhouse and exposed flowering plants to densities of one, three and six fourth-instar larvae of H. armigera, for four days. Leaves, flowers and nectar were analyzed for nicotine, nornicotine and anabasine. The principal leaf alkaloid was nornicotine (mean: 28 µg/g dry mass) followed by anabasine (4.9 µg/g) and nicotine (0.6 µg/g). Nornicotine was found in low quantities in the flowers, but no nicotine or anabasine were recorded. The nectar contained none of the alkaloids measured. Larval growth was reduced when leaves of flowering plants were exposed to six larvae. As predicted by the optimal defense theory, herbivory had a localized effect and caused an increase in nornicotine concentrations in both undamaged top leaves of herbivore damaged plants and herbivore damaged leaves exposed to one and three larvae. The nicotine concentration increased in damaged compared to undamaged middle leaves. The nornicotine concentration was lower in damaged leaves of plants exposed to six compared to three larvae, suggesting that N. africana rather invests in new growth as opposed to protecting older leaves under severe attack. The results indicate that the nornicotine-rich N. africana will be unattractive to herbivores and more so when damaged, but that potential pollinators will be unaffected because the nectar remains alkaloid-free even after herbivory.

Mandibular gland pheromone contents in workers and queens of Apis mellifera adansonii

Secretions from the mandibular glands of honeybees have been studied extensively, with those of queens dominated by ώ-9 fatty acids and ώ-10 fatty acids dominating those of non-laying workers. Apis mellifera adansonii (Latreille) is one of the widely distributed subspecies of African honeybees. However, its mandibular gland pheromones have not been analysed previously. Using gas chromatography, we analysed the composition of mandibular gland pheromones in workers and queens of A. mellifera adansonii from Nigeria. Qualitatively, workers and queens have similar pheromone profiles to those previously reported in other African subspecies of honeybees. We found 9-ODA and high amounts of its precursor 9-hydroxy-2 (E)-decenoic acid (9-HDA) in workers, thus showing that they produce queen-like signals under queen-right conditions. We also found geographic variation in the pheromone profiles and morphometric characters of these workers, suggesting different pheromone and morphoclusters from the different ecological and climatological regions inhabited by A. m. adansonii in Nigeria.

Effects of age and Reproductive Status on Tergal Gland Secretions in Queenless Honey bee Workers, Apis mellifera scutellata and A. m. capensis

Secretions from tergal glands are part of a queen’s pheromonal control of worker reproduction in honey bees. However, in queenless honey bee colonies, workers compete to gain pheromonal, and hence reproductive dominance, over nestmates with ontogenetic changes in their glandular secretions that affect the behavioral or physiological responses of other individuals. Using gas chromatography/mass spectrometry, we investigated for the first time the age-dependent changes in tergal gland secretions of queenless workers of the clonal lineage of Apis mellifera capensis and workers of A. m. scutellata. The reproductive status of honey bee workers was determined by recording the presence of spermathecae and the level of ovarian activation. The tergal gland chemicals identified in both A. m. scutellata workers and A. m. capensis clone workers were oleic acid, n-tricosene,n-pentacosene, and n-heptacosene, with three additional compounds, palmitic acid, n-heneicosene, and n-nonacosene, in A. m. capensis clones. We report ethyl esters as new compounds from honey bee worker tergal gland profiles; these compounds increased in amount with age. All A. m. capensis clone workers dissected had spermathecae and showed ovarian activation from day 4, while ovarian activation only started on day 7 for A. m. scutellata workers that had no spermathecae. Tergal gland secretions were present in higher quantities in bees with activated, rather than inactive ovaries. This suggests that tergal gland secretions from reproductive workers could act as releaser and primer pheromones in synergy with other glandular compounds to achieve pheromonal and reproductive dominance.

Prey choice and raiding behaviour of the Ponerine ant Pachycondyla analis (Hymenoptera: Formicidae)

Termite raiding behaviour of the African poneromorph ant Pachycondyla analis was studied at Mpala, Kenya. In all, 330 raids were observed with the raiding activity showing peaks in the morning and evening. Time spent at the termite source was positively correlated with the numbers of termites taken. The sizes of foraging parties, number of termites taken, distance travelled and time spent at termite sources also showed a positive correlation. Pachycondyla analis preyed significantly more on Microtermes spp. than they did on Odontotermes spp. but no significant differences were found in terms of predator efficiency even though many ants were injured in raids on Odontotermes spp. compared with those on Microtermes spp. Our results indicate that P. analis seems to forage optimally, balancing the costs of energy with prey reward and prey choices were not only influenced by prey abundance, but also by the costs of foraging, as influenced by prey defences, size and foraging behaviour.

An Effective Method for Maintaining the African Termite-Raiding Ant Pachycondyla analis in the Laboratory

Pachycondyla analis Latreille (Hymenoptera: Formicidae) is a common African Ponerine ant that organizes group raids on termites considered a huge burden to agriculture. This ant has been the subject of various entomological and natural history studies aimed at understanding their group raiding behaviour and impact on the ecosystem as well as the roles they play in regulating field termite populations. However, colony maintenance under laboratory conditions for long-term research purposes has largely been unsuccessful. Herein, we report an effective method for maintaining P. analis in the laboratory for long-term studies that may include behavioural, life history and chemical ecology. Using a simple set-up made up of a Perspex foraging arena and an aluminum nest box in the laboratory, queen right colonies were successfully maintained for an average of 27.0 ± 6.0 weeks and a maximum of 34 weeks before declining. High ant mortality (6–48 %) was observed in the first week of captivity in the laboratory. This declined to a weekly mortality of 4.0 ± 3.6 % (24 ± 22.5 ants per colony) after the ants had settled in their new laboratory nest. Therefore, using our laboratory rearing set-up, and keeping laboratory conditions similar to those in the field, as well as feeding P. analis on its usual diet of termites, could increase colony survival time up to 4.5 times longer than previously reported rearing protocols.

Hygienic and grooming behaviors in African and European honeybees - new damage categories in Varroa destructor

Varroa destructor is an ectoparasitic pest of honeybees, and a threat to the survival of the apiculture industry. Several studies have shown that unlike European honeybees, African honeybee populations appear to be minimally affected when attacked by this mite. However, little is known about the underlying drivers contributing to survival of African honeybee populations against the mite. We hypothesized that resistant behavioral defenses are responsible for the survival of African honeybees against the ectoparasite. We tested this hypothesis by comparing grooming and hygienic behaviors in the African savannah honeybee Apis mellifera scutellata in Kenya and A. mellifera hybrids of European origin in Florida, USA against the mite. Grooming behavior was assessed by determining adult mite infestation levels, daily mite fall per colony and percentage mite damage (as an indicator of adult grooming rate), while hygienic behavior was assessed by determining the brood removal rate after freeze killing a section of the brood. Our results identified two additional undescribed damaged mite categories along with the six previously known damage categories associated with the grooming behavior of both honeybee subspecies. Adult mite infestation level was approximately three-fold higher in A. mellifera hybrids of European origin than in A. m. scutellata, however, brood removal rate, adult grooming rate and daily natural mite fall were similar in both honeybee subspecies. Unlike A. mellifera hybrids of European origin, adult grooming rate and brood removal rate did not correlate with mite infestation levels on adult worker honeybee of A. m. scutellata though they were more aggressive towards the mites than their European counterparts. Our results provide valuable insights into the tolerance mechanisms that contribute to the survival of A. m. scutellata against the mite.

Glandular sources of pheromones used to control host workers (Apis mellifera scutellata) by socially parasitic workers of Apis mellifera capensis

Pheromonal control by the honey bee queen is achieved through the use of secretions from diverse glandular sources, but the use of pheromones from a variety of glandular sources by reproductively dominant workers, has not previously been explored. Using the social parasite, Apis mellifera capensis clonal worker we studied the diversity of glandular sources used for pheromonal control of reproductively subordinate A. m. scutellata workers. To determine whether pheromones from different glandular sources are used by reproductively active workers to achieve dominance and evaluate the degree of pheromonal competition between workers of the two sub-species, we housed groups of workers of the two sub-species together in cages and analysed mandibular and tergal gland secretions as well as, ovarian activation status of each worker after 21days. The results showed that A. m. capensis invasive clones used both mandibular and tergal gland secretions to achieve reproductive dominance and suppress ovarian activation in their A. m. scutellata host workers. The reproductively dominant workers (false queens) produced more queen-like pheromones and inhibited ovarian activation in subordinate A. m. scutellata workers. These results show that tergal gland pheromones working in synergy with pheromones from other glands allow individual workers (false queens) to establish reproductive dominance within these social groups and to act in a manner similar to that of queens. Thus suggesting that, the evolution of reproductively dominant individuals (queens or false queens) and subordinate individuals (workers) in social insects like the honey bee is the result of a complex interplay of pheromonal signals from different exocrine glands.

Effect of Brood Pheromone on Survival and Nutrient Intake of African Honey Bees ( Apis mellifera scutellata ) under Controlled Conditions

The influence of pheromones on insect physiology and behavior has been thoroughly reported for numerous aspects, such as attraction, gland development, aggregation, mate and kin recognition. Brood pheromone (BP) is released by honey bee larvae to indicate their protein requirements to the colony. Although BP is known to modulate pollen and protein consumption, which in turn can affect physiological and morphological parameters, such as hypopharyngeal gland (HPG) development and ovarian activation, few studies have focused on the effect of BP on nutritional balance. In this study, we exposed newly emerged worker bees for 14 d and found that BP exposure increased protein intake during the first few days, with a peak in consumption at day four following exposure. BP exposure decreased survival of caged honey bees, but did not affect either the size of the HPG acini or ovarian activation stage. The uncoupling of the BP releaser effect, facilitated by working under controlled conditions, and the presence of larvae as stimulating cues are discussed.