Entomology: Asian honeybees parasitize the future dead

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Vol 437|6 October 2005

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Asian honeybees parasitize the future deadWhen a queen dies, unrelated workers seize the chance to move into her nest and lay their own eggs.

The queen of a honeybee colony has a repro-ductive monopoly because her workers’ovaries are normally inactive and any eggs thatthey do lay are eaten by their fellow workers1–3.But if a colony becomes queenless, the workersstart to lay eggs, stop policing2 and rear a lastbatch of males before the colony finally diesout4. Here we show that workers of the Asiandwarf red honeybee Apis florea from othercolonies exploit this interval as an opportunityto move in and lay their own eggs while nopolicing is in force. Such parasitism of queen-less colonies does not occur in the westernhoneybee A. mellifera and may be facilitatedby the accessibility of A. florea nests, which arebuilt out in the open.

Apis florea are small honeybees that nest bybuilding a single comb attached to a twig(Fig. 1). We collected four wild A. florea nests(one in 2003 and three in 2004) and trans-ported them to a different location that hostsmany wild A. florea colonies, tying them on tolow tree branches at least 5 m away from anyother nest. After taking a sample of workers,we removed the queens from the translocatedcolonies and also any queen cells that subse-quently developed. We sampled adult workersafter one week and again after four weeks(pooled data are shown in Table 1). Samples ofworker-produced eggs, larvae and pupae werecollected as they appeared in the combs (but

not for colonies 3 and 4,as these absconded beforelarvae were reared). Wedissected the adult work-ers to determine theirovary activation3 andused analysis of DNAmicrosatellite loci todetermine their paren-tage and that of worker-produced males3. (Fordetails, see supplemen-tary information.)

Before the queen wasremoved, the number ofunrelated (non-natal)workers in the colonywas low (averaging2.0%; Table 1) and noneof these workers hadactivated ovaries. Afterqueen removal, how-ever, the proportion ofnon-natal workers rosesignificantly (P�0.008)to 4.5%. Significantlymore (P�0.001) non-natal workers (42.6%)had activated ovaries than did natal workers(17.7%), indicating that parasitic workersmay actively seek out queenless colonies inorder to lay eggs. Moreover, non-natal workers

had significantly higher repro-ductive success (P�0.001)than natal workers: 3.2% ofworkers in colonies 1 and 2were non-natal, but these laid35.6% of the eggs and 22.5% of the pupae.

These results show that animportant reproductive tacticof A. florea workers is activelyto seek out and parasitizequeenless nests with their eggs.This behaviour is not evidentin the western honeybee,A. mellifera, in which the off-spring of non-natal workersare rare or absent in queenlessnests5. Our findings could alsoexplain why queenless dwarf-bee colonies often abscondfrom their nests: these workersopt to join new, unrelated nests and parasitize them with their eggs. Even workers from

A. florea colonies that have a queen maychoose to parasitize queenless nests, perhapsbecause they favour individual reproductionin a queenless nest over contributing to thereproductive output of their own colony.Piyamas Nanork*†‡, Jürgen Paar†,Nadine C. Chapman†, Siriwat Wongsiri*,Benjamin P. Oldroyd†*Department of Biology, ChulalongkornUniversity, Bangkok 10330, Thailand†School of Biological Sciences A12, University of Sydney, New South Wales 2006,Australiae-mail: boldroyd@bio.usyd.edu.au‡Department of Biology, MahasarakhamUniversity, Mahasarakham 44150, Thailand

1. Ratnieks, F. L. W. & Visscher, P. K. Nature 342, 796–797(1989).

2. Miller, D. G. & Ratnieks, F. L. W. Insectes Sociaux 48,178–184 (2001).

3. Halling, L. A. et al. Behav. Ecol. Sociobiol. 49, 509–513(2001).

4. Page, R. E. & Robinson, G. E. Behav. Ecol. Sociobiol. 35,99–107 (1994).

5. Martin, C. J., Oldroyd, B. P. & Beekman, M. Behav. Ecol.Sociobiol. 56, 42–49 (2004).

Supplementary information accompanies thiscommunication on Nature’s website.Competing financial interests: declared none.doi:10.1038/437829a

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Figure 1 | Out in the open. The nest of the Asian dwarf red honeybee,Apis florea, is built as a single comb suspended from a twig. This makes itaccessible to workers invading from other colonies when the queen dies.

Table 1 | Reproductive parasitism of queenless colonies

Colony

1 2 3 4Before queen removal

Number of non-natal workers 1 5 0 2

Number of natal workers 99 95 96 94

After queen removal

Number of non-natal workers 0 13 8 14

Number of natal workers 200 187 184 178

Non-natals with activated ovaries (%) – 15.4 62.5 50.0

Natals with activated ovaries (%) 28.0 27.8 4.9 10.1

Offspring derived from non-natal workers (%) (number of offspring sampled)

Eggs 44.4 26.7 – –

(115) (120)

Larvae 38.5 25.6 – –

(143) (125)

Pupae 30.0 14.9 – –

(100) (94)

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