Naturwissenschaften (2001) 88:214–216 DOI 10.1007/s001140100224
S H O R T C O M M U N I C AT I O N
P. Neumann · C. W. W. Pirk · H. R. Hepburn A. J. Solbrig · F. L. W. Ratnieks · P. J. Elzen J. R. Baxter
Social encapsulation of beetle parasites by Cape honeybee colonies (Apis mellifera capensis Esch.) Received: 15 January 2001 / Accepted in revised form: 17 March 2001 / Published online: 10 May 2001 © Springer-Verlag 2001
Abstract Worker honeybees (Apis mellifera capensis) encapsulate the small hive beetle (Aethina tumida), a nest parasite, in propolis (tree resin collected by the bees). The encapsulation process lasts 1–4 days and the bees have a sophisticated guarding strategy for limiting the escape of beetles during encapsulation. Some encapsulated beetles died (4.9%) and a few escaped (1.6%). Encapsulation has probably evolved because the small hive beetle cannot easily be killed by the bees due to its hard exoskeleton and defensive behaviour.
Introduction The small hive beetle, Aethina tumida (SHB), is a parasite of the honeybee (Apis mellifera) endemic to Africa. It lives within honeybee nests and feeds on brood and stored food but seldom causes serious damage (Hepburn and Radloff 1998). On the other hand, the SHB is proving a serious threat to European races of A. mellifera in the south-eastern United States since its introduction in 1998 (Elzen et al. 1999). One possible reason for this difference is that African honeybees sympatric with the SHB have evolved specific defence mechanisms. Unlike other parasites (Moritz et al. 1991), SHB are easily detected and vigorously attacked by the workers in P. Neumann (✉) Martin-Luther-Universität Halle-Wittenberg, Institut für Zoologie/Molekulare Ökologie, Kröllwitzerstrasse 44, 06099 Halle/Saale, Germany e-mail:
[email protected] Tel.: +49-345-5526235, Fax: +49-345-5527037 C.W.W. Pirk · H.R. Hepburn · A.J. Solbrig Department of Zoology and Entomology, Rhodes University, Grahamstown 6140, South Africa F.L.W. Ratnieks Department of Animal and Plant Sciences, Sheffield University, Western Bank, Sheffield S10 2TN, UK P.J. Elzen · J.R. Baxter USDA, Kika de la Garza Subtropical Agricultural Research Center, Weslaco, TX 78596, USA
an African honeybee nest, but it is difficult for the bees to kill or eject them (Lundie 1940; Elzen et al. 2001). Instead the bees encapsulate SHBs in propolis, tree resin which the bees collect and use for sealing cracks in the nest cavity.
Methods Adult male and female small hive beetles, A. tumida (Coleoptera: Nitidulidae), infest honeybee colonies and may stay within them for a long period of time, until they can finally successfully reproduce (Lundie 1940; Schmolke 1974). SHB eggs are laid on the combs and adults as well as the emerging larvae feed on honey, pollen and brood (Lundie 1940; Schmolke 1974; Elzen et al. 1999), although they seem to prefer the latter as their protein diet. After about 14 days the larvae reach the wandering phase (Schmolke 1974), leave the hives and pupate in the soil close to the hive for about 17 days (Lundie 1940; Schmolke 1974). Emerging adults leave the soil and may disperse over large distances to infest new host colonies (unpublished data). In South Africa, successful reproduction of SHB is mainly restricted to small and weak colonies (Lundie 1940); but once larvae emerge, colonies quickly show “wormy” combs (Schmolke 1974, personal observation), due to the high reproductive potential of this parasite. In natural populations SHB show great variation in size (Schmolke 1974) but, in general, male beetles are slightly smaller (length: 5.12±0.07 mm; breadth: 3.21±0.04 mm) than females (length: 5.27±0.06 mm; breadth: 3.25±0.04 mm; Schmolke 1974). In contrast to African honeybees, even strong colonies of European bees are decimated by SHB (Elzen et al. 1999). This is probably caused by high infestation levels, which may be in excess of ~1,000 adult SHB and several hundred larvae per colony (Elzen et al. 1999). Moreover, European honeybees in the New World show significantly less aggressive and investigative contact behaviour towards adult SHB than African A. mellifera
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do (Elzen et al. 2001). This clearly shows that SHB are a serious threat to the European races of A. mellifera. We investigated the encapsulation of SHBs by the Cape honeybee, A. m. capensis, in South Africa where both are endemic. Four colonies (each ~3,000 bees), naturally infested with SHB, were kept in observation hives and monitored daily at 0900 hours and 2000 hours for either 21 (colonies 1 and 2) or 57 days (colonies 3 and 4). We recorded numbers of free and encapsulated SHB, the latter were checked to see if the beetles were dead or alive at the end of the observation period. The frequency of infestation and encapsulation in 40 Langstroth field colonies was determined by counting live SHB throughout the hives. All pieces of propolis were carefully examined for previously encapsulated SHB.
Fig. 1 Social encapsulation of beetle parasites in a Cape honeybee (Apis mellifera capensis) colony, showing two workers keeping a small hive beetle (Aethina tumida) within a confinement area made of propolis
Results SHB were frequently found in small gaps (height: 2–4 mm) between the frame and end bars in the observation hives. As previously reported (Elzen et al. 2001), workers were usually unable to kill the well-armoured SHB; although when two SHBs moved straight into a cluster of workers they were decapitated by the bees. Although a SHB in the open is vigorously attacked by workers, the beetle stays motionless and tucks its head underneath the pronotum with the legs and antennae pressed tightly to the body (much like withdrawal in a turtle). If the workers leave the SHB, the beetle scurries into hiding. We also observed that workers added propolis at the edges of the hive around detected hidden SHBs and completely encapsulated most of them (four managed to escape, see Table 1). The four observation hives contained 15 such propolis prisons (Fig. 1), each confining between 1 and ~200 SHB (12 of which died while in confinement), and 62 free SHB (Table 1). The bees had a sophisticated strategy for hindering beetle escape during encapsulation. While some workers added propolis around the SHB one or more others (mean=2±1.27) continuously guarded the SHB in both open and closed con-
Table 1 Social encapsulation in observation hive and field colonies of the Cape honeybee, Apis mellifera capensis infested with the small hive beetle, Aethina tumida (SHB). Only infested colonies are included; n.d. = not determined, n = number of observed beetles or confinements a The number of escaped and encapsulated SHB could not be precisely determined for one prison in observation colony 4, because about 200 SHB were confined in a small area
Observation hives 2 3 4 Field colonies 2 3 4 5 6 7 8
finements day and night for up to 57 days (Fig. 1). The guard workers continuously tried to attack all SHB when they moved to the edges of still open confinements, and thus kept them imprisoned. It took 1–4 days for the SHB to be encapsulated. Two matings in prisons and one case of cannibalism among SHBs were also observed. A total of 32 free-moving SHBs were found in eight infested field hives. In two of these we also found evidence of encapsulation (Table 1). No SHB larvae were observed in any of the colonies.
Discussion Our data clearly indicate that Cape honeybee colonies use social encapsulation as an efficient defence mechanism against parasitic beetles. Although the A. m. capensis workers vigorously attack small hive beetles, the parasite is seldom harmed, due to its hard exoskeleton and defensive behaviour. Our data also support earlier observations (Schmolke 1974) that SHB typically hide in small cracks in the nest cavity. Thus, social encapsulation by the host has probably evolved in the endemic region of the small hive beetle, as an alternative mecha-
Colony
Free moving SHB (n)
Confinements Encapsulated SHB (n) (n) Alive Dead
Escaped SHB (n)
1 10 23 21 1 1 1 6 2 12 3 4
8 3 1 5 3 0 0 3 0 2 0 0
6 3 12 ~200 0 0 0 3 0 2 0 0
1
32 0 5 7 0 0 0 2 0 1 0 0
0 3 0 n.d.a 0 – – – – – – –
–
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nism to prevent or postpone successful reproduction of the parasite. A total of only 32 free moving SHBs were found in eight out of 40 field hives, suggesting generally low infestation levels in Cape honeybee colonies. We also found evidence of encapsulation in these field colonies, but encapsulation was only seen in the two colonies with the highest numbers of live beetles, suggesting that encapsulation may be triggered when parasite loads reach a threshold. At least four SHB managed to escape encapsulation at night, possibly because honeybees are generally less active at night (Moritz and Kryger 1994). The observed matings and the case of cannibalism among SHBs could well enhance SHB survival in large prisons such as the one in observation colony 4, which held about 200 SHBs. Nevertheless, encapsulation is clearly an effective defence mechanism of honeybees because beetles are prevented from successful reproduction. This seems especially important in light of the high reproductive potential of the SHB (Lundie 1940, unpublished data). Even if some SHB manage to escape, encapsulation provides a prolonged time window for the colonies to prepare for absconding, which is very common in African honeybees and can be triggered by parasites (Hepburn and Radloff 1998). Since the SHB is non-phoretic, absconding leaves the parasites behind. Indeed, the heavily infested observation colony 4 had absconded after 57 days. No SHB larvae appeared even in this nest during this time, indicating that the combination of aggressive behaviour (Elzen et al. 2001) and encapsulation was able
to prevent SHB reproduction even under heavy infestation conditions. We conclude that the social encapsulation of SHBs is another striking example of the co-evolution between insect societies and their parasites. Acknowledgements Appreciation is addressed to A. Flügge, W.R.E. Hoffmann and S. Ranchhod for technical assistance. Financial support was granted by means of a Rhodes University Fellowship (P.N.), the DFG (P.N.), a DAAD fellowship (C.W.W.P.) and by the USDA (H.R.H., P.J.E. and J.R.B.).
References Elzen PJ, Baxter JR, Westervelt D, Randall C, Delaplane KS, Cutts L, Wilson WT (1999) Field control and biology studies of a new pest species, Aethina tumida Murray (Coleoptera, Nitidulidae) attacking honey bees in the Western Hemisphere. Apidologie 30:361–366 Elzen PJ, Baxter JR, Neumann P, Solbrig AJ, Pirk CWW, Hepburn HR, Westervelt D, Randall C (2001) Behavior of African and European subspecies of Apis mellifera toward the small hive beetle, Aethina tumida Murray. J Apic Res (in press) Hepburn HR, Radloff SE (1998) Honeybees of Africa. Springer, Berlin Heidelberg New York Lundie AE (1940) The small hive beetle, Aethina tumida. South Africa Department of Agriculture and Forestry Entomological Series 3, Science Bulletin 220 Moritz RFA, Kryger P (1994) Self organisation of circadian rhythms in groups of honeybees (Apis mellifera L.). Behav Ecol Sociobiol 34:211–215 Moritz RFA, Kirchner M, Crewe RM (1991) Chemical camouflage of the death head hawkmoth, Acherontia atropus. Naturwissenschaften 78:179–182 Schmolke MD (1974) A study of Aethina tumida: the small hive beetle. MS thesis, University of Rhodesia
