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Sympatric Asian honey bee species intercept competitor signals
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The Living Legend

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Sympatric Asian honey bee species intercept competitor signals
07-28-2017 6:29 AM

Foragers of sympatric Asian honey bee species intercept competitor signals by avoiding benzyl acetate from Apis cerana alarm pheromone


While foraging, animals can form inter- and intraspecific social signalling networks to avoid similar predators. We report here that foragers of different native Asian honey bee species can detect and use a specialized alarm pheromone component, benzyl acetate (BA), to avoid danger. We analysed the volatile alarm pheromone produced by attacked workers of the most abundant native Asian honey bee, Apis cerana and tested the responses of other bee species to these alarm signals. As compared to nest guards, A. cerana foragers produced 3.38 fold higher levels of BA. In foragers, BA and (E)-dec-2-en-1-yl acetate (DA) generated the strongest antennal electrophysiological responses. BA was also the only compound that alerted flying foragers and inhibited A. cerana foraging. BA thereby decreased A. cerana foraging for risky sites. Interestingly, although BA occurs only in trace amounts and is nearly absent in sympatric honeybee species (respectively only 0.07% and 0.44% as much in A. dorsata and A. florea), these floral generalists detected and avoided BA as strongly as they did to their own alarm pheromone on natural inflorescences. These results demonstrate that competing pollinators can take advantage of alarm signal information provided by other species.

Alarm signalling, defined as one organism using signals to alert another about danger, is widespread and occurs in plants1, insects2, and vertebrates3, 4. Species at the same trophic level can transfer interspecific information about foraging and risk avoidance5. By using common information that reliably indicates predation, prey may benefit from shared information6, 7. Such information sharing has been demonstrated in tadpoles8, 9, fishes10, and social insects2. This transfer may be beneficial even when the species are competitors. For example, Asian honey bee foragers from different colonies and species can be rivals for limited nectar and pollen resources11. Can they use interspecific alarm pheromones for their individual benefit? Although alarm signalling may be individually costly, it can evolve via kin selection12 and reciprocal altruism13, as exemplified by alarm signals in eusocial organisms. Once such signals have evolved, different colonies of the same species and even different species could benefit by intercepting information about dangerous food locations. Theoretically, they could intercept alarm signal information14. As predicted, A. cerana can use olfactory eavesdropping to detect and avoid an alarm pheromone component in the sympatric Apis dorsata that A. cerana does not possess15.

Such interception within a species is a by-product of colonies having the same alarm pheromone. However, between species with different alarm pheromone compounds or ratios of these compounds, evolution could favour heterospecific sensitivity to alarm pheromones. Species that often encounter each other, like members of a pollinator guild, could benefit by learning to recognize alarm pheromones produced by heterospecifics. This is similar to the phenomenon of bees avoiding heterospecific “footprint” cuticular hydrocarbon odours that indicate a specific flower has already been visited and therefore is less likely to be rewarding16. We hypothesize that different honey bees can learn to associate different honey bee alarm pheromones with danger and thereby reduce their risk of predation during foraging. Such avoidance has implications for pollination, because predators can impose significant non-consumptive effects by causing pollinators to avoid dangerous locations17.

In honey bees, alarm pheromones can increase colony fitness by reducing colony recruitment to dangerous locations. For example, A. mellifera foragers that detected sting alarm pheromone at a food source significantly reduced their recruitment (less waggle dancing) and increased their production of inhibitory stop signals18. Thus, alarm pheromones can also inhibit recruitment communication, providing an olfactory negative feedback signal against the positive feedback signal of the waggle dance.

Honey bee sting alarm pheromones are multi-component blends. Isopentyl acetate (IPA) is the major component of sting alarm pheromone in all honey bee species19. The main other previously-reported sting alarm pheromone components (>10% by mass) of each species are benzyl acetate (BA, in A. mellifera)20, octyl acetate (OA, in A. mellifera, A. cerana, A. florea and A. dorsata)21, (E)-oct-2-en-1-yl acetate (OEA, in A. mellifera)22, (E)-dec-2-en-1-yl acetate (DA, in A. cerana, A. dorsata, A. laboriosa and A. florea)15, 20, 21, 23, (Z)-eicos-11-en-1-ol (EH, in A. mellifera and A. cerana)24, 25, and gamma-octanoic lactone (GOL, in A. dorsata and A. laboriosa)26, 27.

The functions of these different compounds are best understood in the Western honey bee, A. mellifera. IPA, OA and BA play a major role in A. mellifera nest defence. IPA is most important for initiating an alarm response, but is so volatile that it is less effective at marking the intruder for further attacks28. OA is less volatile, and therefore more persistent: it is important for orienting bees towards a moving target28. In A. mellifera, BA is more effective at increasing the number of fanning workers in the hive, which may be part of a defensive response28,29,30. In A. mellifera workers, BA levels also depend upon task specialization22. However, the function of BA is otherwise unclear.

Less is known about the effects of different alarm pheromone components in other honey bee species. IPA is the major alarm pheromone in A. mellifera, A. cerana, A. dorsata, and A. florea, but natural sting pheromone elicits a longer-lasting reaction than IPA alone21. The more persistent DA may provide an orientation cue in A. dorsata and A. florea, as OA does in A. mellifera21, 23. In A. cerana, EH is also more persistent than IPA and may provide orientation information24.

In addition, components may exert different effects depending upon context. In the context of foraging, bees are not defending their colony but rather fleeing from danger and marking a location as dangerous26. For example, GOL and DA are most effective at repelling A. dorsata and A. cerana foragers, even though GOL is not found in A. cerana15. This example of A. cerana intercepting an alarm pheromone component of another bee species illustrates the complexity of forager responses to alarm pheromones15.

A. cerana, A. dorsata, and A. florea are sympatric tropical Asian honey bee species11, 15, face formidable predators at the nest and in the field15, 19, 31,32,33, and are major native pollinators of agricultural crops and native plants in Asia11, 34,35,36,37. The different species vary in population density, with A. cerana as the most common (in order of abundance: A. cerana ≥ A. dorsata > A. florea11, 38). In fact, A. cerana is more than three times more abundant than A. florea38. The abundance of A. dorsata changes seasonally due to their annual migrations. In seasons when A. dorsata is sympatric with A. cerana, A. cerana is initially more abundant than A. dorsata, but A. dorsata eventually becomes as or more abundant than A. cerana11, 38. Thus, it should be advantageous for A. dorsata and A. florea to detect and intercept the alarm pheromone of A. cerana, the most abundant bee species.

Some of these honey bee species have alarm pheromone compounds, like GOL, that are not found in other honey bee species15. However, the primary interspecific differences lie in the relative abundances of these different compounds. Because the relative abundances may be a source of information, it is possible that A. florea and A. dorsata do not respond or respond differently to A. cerana alarm pheromone. Our goal was therefore to better understand the function of different honey bee alarm pheromone components in A. cerana, to determine if BA varies according to A. cerana task specialization, and to test if the sympatric species, A. dorsata and A. florea, can intercept and use this information.

"Perfection is not attainable, but if we chase perfection we can catch excellence."--- Vince Lombardi
07-28-2017 6:29 AM
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