J Biosci (2019) 44:13 Ó Indian Academy of Sciences

DOI: 10.1007/s12038-018-9840-8 (0123456789().,-volV)(0123456789().,-volV)

Nest architecture and colony characteristics of Meliponula (Axestotrigona) ferruginea (, , Meliponini) in Cameroon

1 1 2 MOSES TITA MOGHO NJOYA *, SEINO RICHARD AKWANJOH and DIETER WITTMANN 1Department of Biological Sciences, Faculty of Science, The University of Bamenda, Bamenda, Cameroon 2Institute of Landscape and Ecology, University of Bonn, Bonn, Germany

*Corresponding author (Email, [email protected])

MS received 27 July 2018; accepted 29 November 2018; published online 31 January 2019

Stingless bees have evolved adaptive nest constructions strategies which have resulted in sophisticated nest architecture in many while others lack certain structural components. However, no information exists on the nest biology and ecology on the genus Meliponula in Cameroon. This study aims to contribute to knowledge on the nest architecture and colony characteristics of Meliponula (Axestotrigona) ferruginea. Meliponula ferruginea belongs to the genus Meliponula and subgenus Axestotrigona. This species was first described by Le Peletier De Saini-Farrgeau (1836) and Michener (The bees of the world, The Johns Hopkins University Press, Baltimore and London, 2000) recently. In Cameroon the species has been collected in the northern parts of the country, but there has been no attempt to describe the nest architecture. Our survey from the Bamenda highlands afromontane forests of Cameroon reveals that this species can either nest in tree trunks or in abandoned traditional hollow hives. Interestingly, 50% of colonies studied nested in traditional hollow hives originally baited for honeybees (Apis mellifera adansonii). The nest entrance of Meliponula (Axestotrigona) fer- ruginea ranged from 1 to 1.5 cm (1.2±0.0.24 cm) in diameter, while the external entrance tube extended up to 1.6±0.0.4 cm and the nest entrance tube can go up to 5 cm inward in depending on the thickness of the tree trunk. The nest is made up of sticky brown 5–7 (6±0.98) involucra sheets. The size of brood area depends on the age and condition of the nest. The length of the nest could be between 5.5 and 7.6 cm (6.8±0.98 cm) and up to 13± 4.16 cm combs with a comb diameter of about 7.5±1.29 cm. The cells and storage pots are oval in shape but the storage pots are much larger, about 3 times the size of cell. Generally, this study shows a lot of similarities with other previously studied species in terms of the nest characteristics and measurements. However, the above characteristics can be very useful in taxonomical, phylogenetic and ecological studies of M. ferruginea.

Keywords. Cameroon; Meliponini; Meliponula ferruginea; nest architecture; stingless bees

1. Introduction several hundreds of stingless bee species existing worldwide differ considerably in colony size, body size and color (Michener Stingless bees (Hymenoptera: Apidae) belong to the tribe Meli- 2000). They also vary considerably in their nest architecture with ponini. According to Eardley (2004), 19 species of stingless bees different designs in brood cells arrangements. Brood cells are exist in Africa and they are grouped into six genera. In Camerron, arranged in horizontal or vertical combs, semi-combs or in six species of stingless bees grouped into four genera have been clustered cells. The elaboration of their nest entrance is generally recorded (Njoya 2009). Typically, a meliponine bee colony species-specific. Kajobe and Roubik (2006) affirm that attributes contains approximately 20,000 individuals, comprising of a of the nests are useful in taxonomic studies especially in equa- single fertile queen, drones and workers. They pollinate torial tropical Africa, where little has been studied. Some previ- approximately 90 crop species worldwide (Slaa et al. 2006; ous studies on a major component of the nests of stingless bees Abramson et al. 2007). Stingless bees are known to be generalists have been carried out by Roubik (2006), Eltz et al. (2002), Slaa with regards to selection of nesting sites. The majority of these (2003), and Kajobe and Roubik (2006). bee species build their nests in either tree hollows, abandoned Many species of stingless bees have evolved adaptive nest nests of other social (e.g. ants and termites), which are constructions strategies resulting in sophisticated nest both above- and below-ground environments (Roubik 1980), architecture. For instance, a major component of stingless thereby exhibiting a degree of plasticity in their nesting sites. The bees is the excellent insulation especially in exposed nests. http://www.ias.ac.in/jbiosci 1 13 Page 2 of 7 Njoya MTM et al. This is because several of these species, particularly those of preferences of M. ferruginea is still something to be the moist tropics, are unable to withstand chilling tempera- investigated. tures while others lack certain structural components In Cameroon, Meliponula ferruginea construct their nests (Michener 2000). Nests in large trunks or in soils are also in tree trunks between 1.2 m and 1.5 m above the ground and well insulated (Njoya et al. 2016, 2017a, b). in traditional hollow hives made of raphia bamboos (per- Roubik (1983) observed that the nests of many stingless sonal observation). The two tree trunk nests studied were bee species are yet to be described. This observation is located on trees with circumference of 45 cm and 47 cm especially important for equatorial Africa, where very few respectively. The trees were also located in areas of the studies have been done on stingless bees. savanna forests with few tree canopies which were possibly obstructing direct sunlight rays from reaching the nest entrance. Colonies in traditional hives constructed their nests in a particular area of the hive and the nest cavity was 2. Objectives of the study protected with a batumen lining separating the nest from the rest of the unused area of hive. A nest usually occupies an Due to the lack of information on the biology and ecology of area less than a third of the traditional hive. the stingless bees in Cameroon, we studied the nest char- acteristics of Meliponula ferruginea in the montane forest of the North West Region to describe the nest architecture and 4.2 Nest entrance colony characteristics of this species. The outer tube of the nest entrance can be 2 cm in height with a diameter of 1–1.5 cm. The surrounding of the nest 3. Materials and methods entrance is smeared with propolis. Propolis is a resin-like material made by bees from the exudates gathered from tree The North West Region in Cameroon is situated in the western buds, sap flows, or other botanical sources. Its color varies highlands of Cameroon (figure 1). The region stretches from depending on its botanical source, with dark brown as the 6°200 Northto10°300 South. Stingless bees are distributed all most common. Unlike the nests found on tree trunks, nests over the country and form an important group of pollinators in in traditional hives did not have projections or external agricultural and natural ecosystems. This study was done in entrance. However, their radii remain the same as that of the Donga Mantung and Bui divisions from March to May 2008 nests in tree trunks (figure 4). andFebruarytoApril2017.Twocolonieswerestudiedin2008 The nests in tree trunks (figure 4) have an outer tube at and two in 2017. This followed a survey of bees done in 2007, the nest entrance that can be approximately 2 cm in height during which time stingless bees where collected and identified. with a diameter of 1–1.5cm. Nests in traditional bamboo A sample collection containing pinned Meliponula ferruginea hollow hives (figure 5) have no outer tube projections, in a 12 cm 9 12 cm styrofoam box was used as a guide and and very little propolis outside the entrance compared to presented to farmers, beekeepers and hunters to facilitate nests in tree trunk. Further, entrance in such a nest does recognition of the bees in the various communities where the not lead directly into the brood area but to the batumen. study was done. Nesting sites were found mainly from infor- For nests in tree trunks, no batumen layer was found. mation provided by the hunters, farmers and beekeepers. Four However, the radii of both these types of nests remain the nests of M. ferruginea were studied for details and measure- same. ments. The immediate surroundings of the nests were cleaned and the diameter of the nest entrance measured. The lateral part of the nest was excavated to measure the external part of the 4.3 Nest cavity cavity and its depth measured using a measuring tape. The pollen and the honey pots were counted and the height and The size of a nest cavity of Meliponula ferruginea can be diameter measured using a caliper. The description of the nests between 14 and 17 cm long with a diameter between 6.5 and is done according to Willie (1979). 7.5 cm. The nests found in tree trunks generally were more stretched out (figure 6) than the nests in traditional hollow hives. The size of the nest cavity in tree trunks influenced the 4. Results sizes of the structures in the brood area. The batumen lining, which is a component of the nest cavity of most stingless 4.1 Nesting sites bees, was not found in any of the studied nests of M. ferruginea. A total of four colonies of M. ferruginea were studied, The other structures that can be seen in the nest cavities of 50% of which (two) were in tree trunks in secondary M. ferruginea are the involucra sheets, brood area and the forests (figure 2), while the other (two) 50% were found in storage pots. These structures were found in all the studied traditional hollow hives (figure 3). The exact nesting site nests. Nest architecture of Meliponula Page 3 of 7 13

Figure 1. Map showing the study area. 13 Page 4 of 7 Njoya MTM et al.

Figure 2. A tree trunk with the nest of Meliponula ferruginea. Figure 5. Nest entrance of Meliponula ferruginea in traditional hollow hive.

Figure 3. Nest of Meliponula ferruginea in a traditional hollow bamboo hive: W= wall of traditional hive constructed with bamboos, Ba=Batumen layer surrounding the brood area.

Figure 6. Nest cavity of M. ferruginea in a tree trunk. Portion of trunk removed to expose the nest in the cavity.

4.4 Involucra sheets

The involucra sheets of M. ferruginea cover the brood area. The sheets are sticky and apparently composed of wax and other plant substances. They prevent foreign objects from reaching the brood area directly. The arrangement of the sheets Figure 4. Nest entrance of M. ferruginea in tree trunk: En=ex- is more continuous with nests found in traditional hollow hives ternal entrance tube, Pro=Propolis. (figure 8) than that of the nests in tree trunks (figure 7). Nest architecture of Meliponula Page 5 of 7 13

Cell

Pi

Inv

Pp

Hp a b

Figure 9. (a) Combs of Meliponula ferruginea arranged in horizontal layers with storage pots. (b) Combs of Meliponula Figure 7. Involucra sheets from tree trunk nest surrounding the ferruginea showing pillars between combs. Pi = Pillar,Pp= Pollen brood area. Inv= Involucrum sheet. pot, Hp=Honey pot, Inv = Involucrum.

Figure 8. Involucra sheets from traditional hollow hive surround- Figure 10. Combs of Meliponula ferruginea in tree (Mangifera sp.). ing the brood area. Inv= Involucrum sheets.

The involucra sheets are made up of 5–7 sheets in hives. The cells measured 12 mm high and 3 mm in diameter layers. Each sheet is about 1 mm thick. The sheets are for both type of nests. Most cells are spherical in shape. The attached to each other and to the combs by a 2 mm long storage pots, both the honey and pollen (figure 9a), are mainly pillars. found underneath and above the brood area. The pots are clustered together with similar shape and size.

4.5 Brood area 4.6 Defensive behavior The brood area is made up of cells where the oviposition takes place (brood) and cells that are used as storage pots for Meliponula ferruginea are generally very calm bees. honey and pollen. The brood combs have horizontal However, they are capable of fighting intruders into their arrangements for type of nests and each comb is separated nests by biting and chopping off their wings. This was from one other by a 2 mm pillar (figure 9b). observed with honeybees that were attracted into the nest For both the tree nests and hive nests, the combs were either by spilt honey inside the nests of M. ferruginea.Some- oval, round or heart-shaped with diameter between 7 and 9 cm times the nest entrance was sealed off with propolis to (figure 10). The number of combs per colony could be between prevent any intruder from entering the nest. Generally, 8 and 18. The number of comb per colony depends on the size, these bees are very easy to handle but it is complex to environment and age of the colony. The colonies in tree cavi- investigate tasks related to the process of ovipositioning ties, however, seems to have more combs than the colonies in andprovisioninginartificialhives. 13 Page 6 of 7 Njoya MTM et al.

Table 1. Summary of measurements taken for Meliponula (Axestotrigona) ferruginea

Tree Tree Hive Hive Parameters measured Nest 1 Nest 2 Nest 1 Nest 2 MEAN SD VAR Shape Color Nest Height of external 1.5 2 1.2 1.6 0.4 0.16 entrance entrance (cm) Diameter of nest 1 1.5 1 1.2 1.2 0.24 0.06 entrance (cm) Nest cavity Diameter of nest (cm) 7.5 6.5 5.5 7.6 6.8 0.98 0.97 Length of nest 14 17 14 Batumen Number 1 1 Sticky lining Thickness (cm) 1.2 1.4 1.1 1.5 1.3 0.18 0.03 Brown Involucrum Number 5 6 7 7 6.3 0.96 0.92 Sticky Thickness (cm) 0.1 0.1 0.2 0.13 0.05 0.003 Brown Pillar Length (cm) 0.2 0.1 0.2 0.2 0.18 0.05 0.003 Combs Number of combs 18 14 8 12 13 4.16 17.33 Heart, oval or Diameter of combs 8 9 7 6 7.5 1.29 1.67 circular (cm) Cells Height of cell (cm) 0.3 0.2 0.3 0.3 0.3 0.05 0.003 Oval Diameter (cm) 0.2 0.1 0.2 0.2 0.18 0.05 0.003 Storage Height (cm) 1.2 1.1 1.3 1.3 1.2 0.09 0.01 Spherical pots Diameter (cm) 1 1.1 1 1.1 1.1 0.06 0.003

5. Conclusion Eardley CD 2004 Taxonomic revision of the African stingless bees (Apoidea: Apidae: : Meliponini). African Plant Protect. The nesting site preferences of M. ferruginea areontreetrunks 10 63–96 in secondary forests as well as in traditional hollow bamboo Eltz T, Carsten AB, Van der Kaars S and Linsenmair EK 2002 hives placed in forests. For our studies, we selected two nests in Determinants of sting-less bee nest density in lowland diptero- tree trunks in secondary forests as well as two nests in tradi- carp forests of Sabah, Malaysia. Oecologia 131 27–34 Kajobe R and Roubik DW 2006 Honey-making bee colony tional bamboo hollow hives. The measurements of the various abundance and predation by apes and humans in a Uganda forest parameters are presented in table 1. reserve. Biotropica 38 210–218 The shape, color and rigidity of nest entrance of M. ferruginea Le Peletier De Saini-Farrgeau ALM 1836 Histoire naturelle des varied slightly between colonies. The nest entrance properties of Insectes stingless bees are related to many factors, such as age of nest, Michener CD 2000 The bees of the world (The Johns Hopkins microclimate, predators, parasites, and symbionts (Roubik University Press: Baltimore and London) 2006), as was observed with M. ferruginea. Among the different Njoya MTM 2009 Diversity of stingless bees in Bamenda afromon- characteristics measured, this species showed some peculiarities tane forests –Cameroon: Nest architecture, behaviour and labour in Cameroon. Understanding the nesting preferences of such calendar. Dissertation, Hohen Landwirtschaftlichen Fakulta¨t der bees might not only help in conserving them but also to set up Rheinischen Friedrich-Wilhelms-Universita¨t zu Bonn additional hives by providing the right kind of artificial nesting Njoya MTM, Wittmann D and Ambebe TF 2016 Nest Architecture spaces. Given that these bees are important pollinators, making of Dactylurina Staudingeri (Hymenoptera, Apidae, Meliponini) in Cameroon. Int. J. Res. Agric. Sci. 3 2348–3997 artificial hives could facilitate crop pollination and thereby Njoya MTM, Wittmann D and Balgah RA 2017a Subterranean enhance food security. Nest Architecture and Colony Characteristics of Meliponula (Meliplebeia) becarii (Hymenoptera, Apidae, Meliponini) in Cameroon. J. Chem. Bio. Phy. Sci. 7 220–233 Acknowledgements Njoya MTM, Wittmann D and Anjah GM 2017b Recruitment communication strategy of workers of Dactylurina staudingeri The authors are thankful to the hunters and beekeepers in the (Hymenoptera, Apidae, Meliponini) in Cameroon. JCBPS 7 study area for their assistance in locating nesting sites of M. 234–242 ferruginea and to David Roubik for identification of the bees. Roubik DW 1980 Foraging behaviour of competing Africanized honey bees and stingless bees. Ecology 61 836–845 Roubik DW 1983 Nest and colony characteristics of stingless bees from Panama. J. Kansas Entomol. Soc. 56 327–335 References Roubik DW 2006 Stingless bee nesting biology. Apidologie 37 124–143 Abramson CI, Mixson TA, Cakmak I, Place AJ and Wells H 2007 Slaa J 2003 Foraging ecology of stingless bees: From individual Determinants of sting-less bee nest density in lowland diptero- behaviour to community ecology. Dissertation Utrecht Univer- carp forests of Sabah, Malaysia. Oecologia. 131 22927–22934 sity, Dissertation, Elinkwijk, Utrecht, The Netherlands Nest architecture of Meliponula Page 7 of 7 13 Slaa EJ, Chaves LAS, Malagodi-Braga KS and Hofstede FE 2006 Willie A 1979 Phylogeny and relationships among the genera and Stingless bees in applied pollination: practice and perspectives. subgenera of the stingless bees (Meliponine) of the world. Rev. Apidologie 37 293–315 Biol. Trop. 27 241–277

Corresponding editor: BJ RAO