Foraging and feeding are independently regulated by social and personal hunger in the clonal raider ant

Behavioral Ecology and Sociobiology volume 75, Article number: 41 (2021) Cite this article

Abstract

Ant colonies must assess the internal states of their members and coordinate their responses to changes in state. One important example of this is the sensing of colony hunger and the regulation of foraging behavior. In many ant species, workers’ own nutritional states at least partially determine how much they forage, and poorly nourished workers usually forage more, while well-nourished workers remain inside the nest. Workers in some species, such as the clonal raider ant Ooceraea biroi, mostly forage in response to larval signals. Here, we ask whether O. biroi larvae directly affect worker nutrition, and whether nutritional states in turn regulate workers’ foraging and feeding behavior. We find that larval signals do not detectably influence workers’ nutritional states or feeding behavior. Unlike in most other ant species, however, when colonies forage in response to larval signals, better-nourished O. biroi workers forage more. This suggests evolutionary modifications to the nature and strength of the relationship between nutritional state and foraging behavior in some ants. Nonetheless, worker nutritional states regulate feeding behavior as expected, with workers eating in proportion to their level of food deprivation. We discuss the implications of these results for the life history of O. biroi and the evolution of foraging regulation in social insects more generally. We suggest that the decoupling of regulatory mechanisms for feeding and foraging has parallels in the evolutionary elaboration of animal multicellularity.

Significance statement

Foraging in social insects is a cooperative behavior: workers forage for the colony, rather than just for themselves. In most species, workers primarily use their own hunger as proxies for the colony’s needs. However, some species use other sources of information. Clonal raider ants, for example, forage in response to signals from their larvae. Here, we ask whether they also forage when deprived of nutrition. Surprisingly, we find instead that they forage more when better fed, and that in unmanipulated colonies, larval signals override worker nutrition, suggesting that the regulation of foraging has been rewired in this species. We also find that workers feed in proportion to their nutrient deprivation, suggesting that the regulation of feeding has been conserved. We propose that the uncoupling of feeding and foraging machinery has parallels in the evolutionary elaboration of animal multicellularity.

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Data availability

All analysis code and data is available on GitHub. DOI: https://doi.org/10.5281/zenodo.4473344.

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Acknowledgements

We thank Leonora Olivos-Cisneros and Stephany Valdés Rodríguez for assistance with ant maintenance; Amelia Ritger, Lavoisier Ramos-Espiritu, and the Rockefeller University High-Throughput Screening Resource Center for assistance with assay development; Asaf Gal for assistance with automated behavioral tracking; Hua Yan for suggesting the lipid quantification method; and Audrey Dussutour, Abel Bernadou, Adria LeBoeuf, Lior Baltiansky, and the entire Kronauer lab for helpful discussion.

Funding

This work was supported by a Faculty Scholars Award from the Howard Hughes Medical Institute to D.J.C.K. This is Clonal Raider Ant Project paper #17.

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  1. Vikram Chandra

    Present address: Department of Organismic and Evolutionary Biology, Harvard University, 52 Oxford Street, Cambridge, MA, 02138, USA

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  1. Laboratory of Social Evolution and Behavior, The Rockefeller University, 1230 York Avenue, New York, NY, 10065, USA

    Vikram Chandra & Daniel J. C. Kronauer

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Chandra, V., Kronauer, D.J.C. Foraging and feeding are independently regulated by social and personal hunger in the clonal raider ant. Behav Ecol Sociobiol 75, 41 (2021). https://doi.org/10.1007/s00265-021-02985-7

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Keywords

  • Eusociality
  • Formicidae
  • Nutrition
  • Social behavior
  • Social insects