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“The Cape Honeybee, Apis Mellifera Capensis Esch “Inter- and intraspecific parasitism in honeybees (Apis mellifera L.): the small hive beetle (Aethina tumida Murray) and the Cape honeybee (A. m. capensis Esch.)” H a b i I i t a t i o n s s c h r i f t zur Erlangung des akademischen Grades Dr. rer. nat. habil. vorgelegt der Mathematisch – Naturwissenschaftlich - Technischen Fakultät der Martin-Luther Universität Halle-Wittenberg von Herrn Dr. rer. nat. Peter Neumann Geb. am: 14.12.1967 in: Berlin Gutachter /in 1. Prof. Dr. Robin FA Moritz 2. Prof. Dr. Jürgen Tautz 3. Prof. Dr. Michael P Schwarz Halle (Saale), den 14.07.2004 urn:nbn:de:gbv:3-000007748 [http://nbn-resolving.de/urn/resolver.pl?urn=nbn%3Ade%3Agbv%3A3-000007748] Contents 1 Introduction 3 2 The small hive beetle (Aethina tumida Murray, Coleoptera: Nitidulidae) 4 2.1 Laboratory rearing of small hive beetles Aethina tumida (Coleoptera, Nitidulidae) 9 2.2 Longevity and reproductive success of Aethina tumida (Coleoptera: Nitidulidae) fed different natural 11 diets 2.3 The effects of adult small hive beetles, Aethina tumida (Coleoptera: Nitidulidae), on nests and flight 17 activity of Cape and European honey bees (Apis mellifera) 2.4 Behaviour of African and European subspecies of Apis mellifera toward the small hive beetle, Aethina 25 tumida 2.5 Social encapsulation of beetle parasites by Cape honeybee colonies (Apis mellifera capensis Esch.) 27 2.6 Cape (Apis mellifera capensis) and European (Apis mellifera) honey bee guard age and duration of 30 guarding small hive beetles (Aethina tumida) 2.7 Removal of small hive beetle (Aethina tumida Murray) eggs and larvae by African honeybee colonies 34 (Apis mellifera scutellata Lepeletier) 2.8 The biology of the small hive beetle, Aethina tumida Murray (Coleoptera: Nitidulidae): Gaps in our 39 knowledge of an invasive species 3 The Cape honeybee (Apis mellifera capensis Esch.) 54 3.1 A method for estimating variation in the phenotypic expression of morphological characters by 59 thelytokous parthenogenesis in Apis mellifera capensis 3.2 Modes of worker reproduction, reproductive dominance and brood cell construction in queenless 65 honeybee (Apis mellifera L.) colonies 3.3 Social parasitism by honeybee workers (Apis mellifera capensis Esch.): Host finding and resistance of 69 hybrid host colonies 3.4 Absconding in honeybees (Apis mellifera) in relation to queen status and mode of worker reproduction 85 3.5 A scientific note on the natural merger of two honeybee colonies (Apis mellifera capensis Esch.) 89 3.6 The behaviour of drifted Cape honeybee workers (Apis mellifera capensis Esch.): predisposition for 91 social parasitism? 3.7 Cape honeybees, Apis mellifera capensis, police worker-laid eggs despite the absence of relatedness 95 benefits 3.8 Spatial differences in worker policing facilitate social parasitism of Cape honeybee workers (Apis 103 mellifera capensis Esch.) in queenright host colonies 3.9 Egg laying and egg removal by workers are positively correlated in queenright Cape honeybee colonies 108 (Apis mellifera capensis Esch.) 3.10 Parasitic Cape bees in the northern regions of South Africa: source of the founder population 113 3.11 Behavioural basis for social parasitism of Cape honeybees (Apis mellifera capensis Esch.) 118 3.12 The Cape honeybee phenomenon: the sympatric evolution of a social parasite in real time? 136 2 1 Introduction Honeybees, Apis mellifera, are eusocial insects with a well developed reproductive division of labour between the queen and the workers (Wilson, 1971). While, the queen usually dominates reproduction, the workers participate in all other tasks necessary to maintain the colony, e.g. brood rearing, foraging and nest defence (Ribbands, 1953). Honeybee colonies comprise of a single egg-laying queen, several thousand workers (~10,000 to 60,000) and several hundred male sexuals (= drones) depending on the season (Moritz and Southwick, 1992). Honeybees naturally nest in cavities, e.g. in hollow trees. The nest is constructed of wax, which is produced in special glands by the workers (Hepburn, 1986). It consists of a central brood nest with a surrounding pollen storage area and a honey storage area in the nest periphery (Ribbands, 1953). The individual bees as well as the colony and its stored resources can be exploited by a wide range of parasitic organisms (Schmid-Hempel, 1998). Parasitism can be defined as the relationship between two organisms, where one organism lives at the expense of another organism, its host. Although parasites do not normally kill their hosts, many of these parasitic associations produce pathological changes in the hosts. In extreme cases, this always results in the death of the host (parasitoids, Schmid-Hempel, 1998). One can distinguish between several forms of parasitism. For example parasitism can occur within a single species (intraspecific) and between two species (interspecific; Schmid-Hempel, 1998). Social parasitism is a common and intriguing phenomenon in social insects. Social parasitic species evolve from their social ancestors by developing mechanisms to exploit the resources of their social hosts. Social parasitism can occur both within and between species (Rinderer et al., 1985; Roubik, 1989). There are several forms of social parasitism (Wilson, 1971; Hölldobler and Wilson, 1990). In some cases workers raid the nests of their own or other species to take food resources (e.g. robbing behaviour of honeybees, Ribbands, 1953; Moritz and Southwick, 1992). Some species show only temporary social parasitism in the nest-founding phase, when mated queens usurp the nests of host species instead of establishing nests by themselves (e.g. wood ants of the genus Formica; Hölldobler and Wilson, 1990). Other species take slaves by stealing brood from hosts` nests (Hölldobler and Wilson, 1990). The host brood is raised in the slave maker nest and performs all tasks necessary for the maintenance of the parasite colony. An advanced form of social parasitism are inquiline species, where the worker caste is either reduced or has been lost altogether (Hölldobler and Wilson, 1990). Some of such species spend their entire life in the host nest (Hölldobler and Wilson, 1990). Social parasite species are often closely related to their hosts (= Emery’s rule, Emery, 1909). This might be related to the communication between host and parasite. In order to successfully pass the host defence mechanism, social parasites must have evolved communication systems, which are very similar to their host species. In recent decades, the frequency of biological invasions has increased to an unprecedented level (Hänfling and Kollmann, 2002). Parasites may also become invasive species, which are transferred from their endemic range into new areas and may cause substantial damage to local ecosystems and agriculture. However, the successful treatment and control of invasive parasite species requires not only comprehensive information about the biology of the parasite itself but also a good understanding of the nature of the parasites' interactions with their hosts species. In the following thesis two recent examples of invasive honeybee parasites were investigated in detail: The small hive beetle and the Cape honeybee. References Emery C (1909) Über den Ursprung der dulotischen, parasitischen und myrmekophilen Ameisen. Biol Zentralbl 29: 352-362. Hölldobler B, Wilson EO (1990) The Ants. Springer Verlag, Berlin, Heidelberg, New York. Hänfling B, Kollmann J (2002) An evolutionary perspective of biological invasions, Trends Ecol. Evol. 17, 545- 546. Moritz RFA, Southwick EE (1992) Bees as superorganisms. An evolutionary reality. Springer Verlag, Berlin, Heidelberg, New York. Ribbands CR (1953) The behaviour and social life of honeybees, Bee Research Association Limited, London, UK. Rinderer TE, Hellmich RL, Danka RG, Collins AM (1985) Male reproductive parasitism. A factor in the Africanization of honeybee populations. Science 228, 1119-1121. Roubik DW (1989) Ecology and natural history of tropical bees. Cambridge, Cambridge University Press. Wilson EO (1971) The insect societies. Cambridge, Harvard University Press. 3 2. The small hive beetle (Aethina tumida Murray, Coleoptera: Nitidulidae) The small hive beetle, Aethina tumida, was first described in 1867 (Murray, 1867) and belongs to the coleopteran family Nitidulidae which contains approximately 2,800 described species in 172 genera worldwide (Habeck, 2002). This family can be distinguished from other similar beetles by their transverse procoxal cavities, grooved metacoxae, dilated tarsal segments, small fourth tarsi and three-segmented antennal club (Habeck, 2002). The Nitidulid beetles can feed on fresh, rotten and dried fruits, plant juices, carrion and crops but occasionally on flowers as well (Lin et al., 1992; Fadamiro et al., 1998; Hepburn and Radloff, 1998; Smart and Blight, 2000; Wolff et al., 2001). Small hive beetles are honeybee parasites native to sub-Saharan Africa, where they are a minor pest only (Lundie, 1940; Schmolke, 1974; Hepburn and Radloff, 1998). In contrast, the beetles can be harmful parasites of European honeybee subspecies (Elzen et al., 1999a,b; Hood, 2000). Since 1998, the small hive beetle has raised considerable international attention because it has become an invasive species in populations of European-derived honeybees in the USA (Elzen et al., 1999a,b) and Australia (Minister for Agriculture, 2002). At present, the effects of beetle infestations seem to be different in the USA and Australia. While even strong colonies of European honeybee subspecies can be taken over and killed by small hive beetles in the USA (Elzen et al., 1999a,b), strong colonies are not affected in Australia (D Anderson, personal communication). The natural history of A. tumida was described by Lundie (1940, 1951, 1952a,b) and Schmolke (1974). The adults are about 5 to 7 mm long, 3 to 4.5 mm wide and are dark brown to black in colour (Lundie, 1940; Schmolke, 1974). Adults are lighter in colour just after pupation (yellowish to red) but soon become darker (Lundie, 1940). Females (length: 5.27 +/-0.06mm; breadth 3.25 +/-0.04 mm) tend to be bigger than males (length: 5.12 +/- 0.07 mm; breadth: 3.21 +/- 0.04 mm; Lundie, 1940).
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