Introduced species and the olfactory landscape of foraging

By Ros Gloag

A blog post about the work of the Insectes Sociaux’s 2021 Best Paper Award “Australian stingless bees detect odours left at food sources by nestmates, conspecifics and honey bees”, by Rosalyn Gloag, Jordan P Smith, Ruby E Stephens, Tim A Heard and Madeleine Beekman, Insect Soc 68:151–159.

My colleagues and I received a lovely email this month to tell us that our paper had been selected for the Insectes Sociaux Best Paper Award 2021 by the Editorial Board. We couldn’t be happier to know that Australia’s amazing stingless bees are getting a bit of a spotlight!

This project arose from the combination of two lines of questioning. The first was a desire to better understand how Australian stingless bees (Tetragonula spp and Austroplebia spp) recruit their nestmates to profitable food sources. When people think of nestmate recruitment in social bees, they are likely to think of the famous waggle dance of honey bees (Apis sp.). Honey bee foragers encode information on the location of food sources in a dance, which they perform inside the darkened nest to their sisters. Stingless bees, meanwhile, have no special dance and yet are nevertheless very efficient recruiters. How do they do it? Studies of stingless bee species in South and Central America have shown that they regularly use pheromones or other odours at, or near, food sources to help guide nestmates to food. There is a relative dearth of information, however, about the recruitment mechanisms used by stingless bees in other parts of their global tropical distribution.

Honey bees and Tetragonula clypearis feeding at an artificial feeder (not as part of the study discussed here, but this photo still illustrates nicely their willingness to co-feed and the relative size of each species! (photo. R. Gloag)

Our second line of questioning involved the possible impacts of introduced bees on native bees in the ecosystems they invade. In Australia, honey bees are not native. They were brought to the continent in 1822 for beekeeping, and later naturalized throughout Australian bushland. In recent years, I have spent a lot of time studying feral Apis populations in Australia and a common question from the public is whether honey bees here impact native bees in any way. I always explain to them that scientists are very interested in this too, but that it is not an easy question to answer because any impacts are likely to be indirect (e.g. competition for resources or nest sites). Honey bees today are hugely abundant in Australian ecosystems and it is common to see them foraging on the same flowers as stingless bees and other native bees. We know that bees can detect the odours of sympatric species at flowers when foraging, but does this apply also to cases where one species is a recent invader? Do Australia’s native bees either avoid or prefer flowers that carry the “whiff” of a honey bee? If so, this could be one avenue by which introduced Apis indirectly affect the foraging ecology of native bees.

We decided to test this idea with very simple binary choice trials (see Figure 1 from the paper). In these trials, foraging stingless bees must choose between identical feeders: one of which has been previously used by other bees (that is, walked all over and potentially odour-marked) and one of which is unused (that is, clean of any bee odours). The first trials were completed in Tetragonula carbonaria by Jordan Smith as part of his undergraduate Honours project (just one of the great things he did – the other was to estimate the species foraging range here). These first trials were very interesting, clearly we needed to continue.

The beautiful spiral brood comb of Tetragonula carbonaria, one of Australia’s endemic stingless bees. (photo. R. Gloag)

Over the next few field seasons, I continued with additional trials. Ruby Stephens lent a hand once she had wrapped up her own Honours project (a great study of nestmate recognition in T. carbonaria – find it here). Progress was not fast; there were interruptions for maternity leaves, new jobs, COVID. Eventually though we had an analyzed dataset for three species of Australian stingless bee (Tetragonula carbonaria, Tetragonula clypearis and Austroplebia australis – representing the three major clades of stingless bees in Australia) each tested in foraging choice trials against the odours of nestmates, non-nestmate conspecifics and honey bees. All three species preferred feeders previously used by other bees, even honey bees, consistent with being able to detect food-marking odours and use these in their foraging decisions. We also tested two of the species (T. carbonaria and A. australis) in choice trials offering feeders marked with vanilla vs no-odour and found no forager preference, indicating it is not simply that stingless bees prefer the smelliest feeder, or that they are attracted to all novel odours.

So stingless bees in Australia use odours at food sources as part of their recruitment strategy, just like their Neotropical relatives. Those odours might be either pheromones, chemical “footprints” or a mix of the two. They also can detect and respond to honey bee odours (almost certain to be footprints in that case). What does it mean that stingless bee foragers were attracted to food sources marked with honey bee odours? My view is that it shows that stingless bees are highly adaptable foragers that can readily learn that any particular odour signals food. I suspect responses to honey bee odours might differ in different contexts, though this remains to be tested. Certainly we are left now with a whole range of new questions: How does the ability to detect the odours of introduced species impact native bee foraging in natural contexts? Do honey bees also respond to the odours of stingless bees? More broadly, how do social insects respond to the pheromones of introduced species that share their ecological space and trophic level?

We thank again the Insectes Sociaux Editorial Board for bestowing on this study the Best Paper 2021 Award, and look forward to learning more about stingless bee foraging ecology in the future.

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