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

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.

References

  1. Avery L, You YJ (2012) C. elegans feeding. In: WormBook: The online review of C. elegans biology [Internet]. Pasadena (CA), pp 1–23

  2. Bazazi S, Arganda S, Moreau M, Jeanson R, Dussutour A (2016) Responses to nutritional challenges in ant colonies. Anim Behav 111:235–249

    Google Scholar 

  3. Behmer ST (2009) Animal behaviour: feeding the superorganism. Curr Biol 19:R366–R368

    CAS  PubMed  Google Scholar 

  4. Bernadou A, Schrader L, Pable J, Hoffacker E, Meusemann K, Heinze J (2018) Stress and early experience underlie dominance status and division of labour in a clonal insect. Proc R Soc B Biol Sci 285:20181468

    Google Scholar 

  5. Bernadou A, Hoffacker E, Pable J, Heinze J (2020) Lipid content influences division of labour in a clonal ant. J Exp Biol 223:jeb219238

    PubMed  Google Scholar 

  6. Blanchard GB, Orledge GM, Reynolds SE, Franks NR (2000) Division of labour and seasonality in the ant Leptothorax albipennis: worker corpulence and its influence on behaviour. Anim Behav 59:723–738

    CAS  PubMed  Google Scholar 

  7. Borowiec M (2016) Generic revision of the ant subfamily Dorylinae (Hymenoptera, Formicidae). Zookeys 608:1–280

    Google Scholar 

  8. Borowiec ML, Rabeling C, Brady SG, Fisher BL, Schultz TR, Ward PS (2019) Compositional heterogeneity and outgroup choice influence the internal phylogeny of the ants. Mol Phylogenet Evol 134:111–121

    PubMed  Google Scholar 

  9. Calderone NW, Johnson BR (2002) The within-nest behaviour of honeybee pollen foragers in colonies with a high or low need for pollen. Anim Behav 63:749–758

    Google Scholar 

  10. Camazine S (1993) The regulation of pollen foraging by honey bees: how foragers assess the colony’s need for pollen. Behav Ecol Sociobiol 32:265–272

    Google Scholar 

  11. Cassill DL, Tschinkel WR (1995) Allocation of liquid food to larvae via trophallaxis in colonies of the fire ant, Solenopsis invicta. Anim Behav 50:801–813

    Google Scholar 

  12. Cassill DL, Tschinkel WR (1999) Information flow during social feeding in ant societies. In: Detrain C, Deneubourg JL, Pasteels JM (eds) Information Processing in Social Insects. Birkhäuser Basel, Basel, pp 69–81

    Google Scholar 

  13. Chandra V, Fetter-Pruneda I, Oxley PR, Ritger AL, McKenzie SK, Libbrecht R, Kronauer DJC (2018) Social regulation of insulin signaling and the evolution of eusociality in ants. Science 361:398–402

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Cornelius ML, Grace JK (1997) Influence of brood on the nutritional preferences of the tropical ant species, Pheidole megacephala (F.) and Ochetellus glaber (Mayr). J Entomol Sci 32:421–429

    Google Scholar 

  15. Crossley M, Staras K, Kemenes G (2018) A central control circuit for encoding perceived food value. Sci Adv 4:eaau9180

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Csata E, Dussutour A (2019) Nutrient regulation in ants (Hymenoptera: Formicidae): a review. Myrmecol News 29:111–124

    Google Scholar 

  17. Daugherty THF, Toth AL, Robinson GE (2011) Nutrition and division of labor: Effects on foraging and brain gene expression in the paper wasp Polistes metricus. Mol Ecol 20:5337–5347

    CAS  PubMed  Google Scholar 

  18. Dejean A (1986) Effect of starvation on the predatory behavior of Serrastruma serrula (Formicidae, Myrmicinae). Sociobiology 13:119–132

    Google Scholar 

  19. Dussutour A, Simpson SJ (2009) Communal nutrition in ants. Curr Biol 19:740–744

    CAS  PubMed  Google Scholar 

  20. Dussutour A, Simpson SJ (2012) Ant workers die young and colonies collapse when fed a high-protein diet. Proc R Soc B Biol Sci 279:2402–2408

    CAS  Google Scholar 

  21. Fiocca K, Capobianco K, Fanwick E, Moynahan K, Congdon R, Zelanko P, Velinsky D, O’Donnell S (2020) Reproductive physiology corresponds to adult nutrition and task performance in a Neotropical paper wasp: a test of dominance-nutrition hypothesis predictions. Behav Ecol Sociobiol 74:114

    Google Scholar 

  22. Fischer EK, O’Connell LA (2017) Modification of feeding circuits in the evolution of social behavior. J Exp Biol 220:92–102

    PubMed  Google Scholar 

  23. Fourcassié V, Bredard C, Volpatti K, Theraulaz G (2003) Dispersion movements in ants: spatial structuring and density-dependent effects. Behav Process 63:33–43

    Google Scholar 

  24. Fowler HG (1980) Populations, prey capture and sharing, and foraging of the Paraguayan ponerine Odontomachus chelifer Latreille. J Nat Hist 14:79–84

    Google Scholar 

  25. Gal A, Saragosti J, Kronauer DJC (2020) anTraX: a software package for high throughput video tracking of color-tagged insects. Elife 9:e58145

    PubMed  PubMed Central  Google Scholar 

  26. Garnier S, Kronauer DJC (2017) The adaptive significance of phasic colony cycles in army ants. J Theor Biol 428:43–47

    PubMed  Google Scholar 

  27. Gotwald WH (1995) Army ants: the biology of social predation. Cornell University Press, Ithaca

  28. Greenwald EE, Baltiansky L, Feinerman O (2018) Individual crop loads provide local control for collective food intake in ant colonies. Elife 7:e31730

    PubMed  PubMed Central  Google Scholar 

  29. Heiden MGV, Cantley LC, Thompson CB (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324:1029–1033

    Google Scholar 

  30. Hölldobler B (1971) Recruitment behavior in Camponotus socius (Hym. Formicidae). Z Vgl Physiol 75:123–142

    Google Scholar 

  31. Hölldobler B, Wilson EO (1990) The ants. Belknap Press, Cambridge

  32. Hölldobler B, Wilson EO (2009) The superorganism: the beauty, elegance, and strangeness of insect societies. W. W. Norton & Company, New York

  33. Howard DF, Tschinkel WR (1980) The effect of colony size and starvation on food flow in the fire ant, Solenopsis invicta (Hymenoptera: Formicidae). Behav Ecol Sociobiol 7:293–300

    Google Scholar 

  34. Judd T (2006) Relationship between food stores and foraging behavior of Pheidole ceres (Hymenoptera: Formicidae). Ann Entomol Soc Am 99:398–406

    Google Scholar 

  35. Kitaoka TK, Nieh JC (2009) Manuscript in preparation for Behavioral Ecology and Sociobiology Bumble bee pollen foraging regulation: role of pollen quality, storage levels, and odor. Behav Ecol Sociobiol 63:501–510

    Google Scholar 

  36. Kronauer DJC (2020) Army ants: nature’s ultimate social hunters. Harvard University Press, Cambridge

  37. Kronauer DJC, Pierce NE, Keller L (2012) Asexual reproduction in introduced and native populations of the ant Cerapachys biroi. Mol Ecol 21:5221–5235

    PubMed  Google Scholar 

  38. Lanan M (2014) Spatiotemporal resource distribution and foraging strategies of ants (Hymenoptera: Formicidae). Myrmecol News 20:53–70

    PubMed  PubMed Central  Google Scholar 

  39. Libbrecht R, Oxley PR, Kronauer DJC (2018) Clonal raider ant brain transcriptomics identifies candidate molecular mechanisms for reproductive division of labor. BMC Biol 16:89

    PubMed  PubMed Central  Google Scholar 

  40. Ma R, Villar G, Grozinger C, Rangel J (2018) Larval pheromones act as colony-wide regulators of collective foraging behavior in honeybees. Behav Ecol 29:1132–1141

    Google Scholar 

  41. Mailleux AC, Detrain C, Deneubourg JL (2006) Starvation drives a threshold triggering communication. J Exp Biol 209:4224–4229

    PubMed  Google Scholar 

  42. Mailleux A-C, Devigne C, Deneubourg J-L, Detrain C (2010) Impact of starvation on Lasius niger’ exploration. Ethology 116:248–256

    Google Scholar 

  43. Markiewicz D, O’Donnell S (2001) Social dominance, task performance and nutrition: implications for reproduction in eusocial wasps. J Comp Physiol A Sensory, Neural, Behav Physiol 187:327–333

    CAS  Google Scholar 

  44. Mayack C, Naug D (2013) Individual energetic state can prevail over social regulation of foraging in honeybees. Behav Ecol Sociobiol 67:929–936

    Google Scholar 

  45. McGrannachan CM, Lester PJ (2013) Temperature and starvation effects on food exploitation by Argentine ants and native ants in New Zealand. J Appl Entomol 137:550–559

    Google Scholar 

  46. Molet M, Chittka L, Stelzer RJ, Streit S, Raine NE (2008) Colony nutritional status modulates worker responses to foraging recruitment pheromone in the bumblebee Bombus terrestris. Behav Ecol Sociobiol 62:1919–1926

    Google Scholar 

  47. Oxley PR, Ji L, Fetter-Pruneda I, McKenzie SK, Li C, Hu H, Zhang G, Kronauer DJC (2014) The genome of the clonal raider ant Cerapachys biroi. Curr Biol 24:451–458

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Pankiw T (2004) Brood pheromone regulates foraging activity of honey bees (Hymenoptera: Apidae). J Econ Entomol 97:748–751

    PubMed  Google Scholar 

  49. Pool A-H, Scott K (2014) Feeding regulation in Drosophila. Curr Opin Neurobiol 29:57–63

    CAS  PubMed  Google Scholar 

  50. Ravary F, Jaisson P (2002) The reproductive cycle of thelytokous colonies of Cerapachys biroi Forel (Formicidae, Cerapachyinae). Insect Soc 49:114–119

    Google Scholar 

  51. Ravary F, Jahyny B, Jaisson P (2006) Brood stimulation controls the phasic reproductive cycle of the parthenogenetic ant Cerapachys biroi. Insect Soc 53:20–26

    Google Scholar 

  52. Rion S, Kawecki TJ (2007) Evolutionary biology of starvation resistance: what we have learnt from Drosophila. J Evol Biol 20:1655–1664

    CAS  PubMed  Google Scholar 

  53. Robinson EJH, Richardson TO, Sendova-Franks AB et al (2008) Radio tagging reveals the roles of corpulence, experience and social information in ant decision making. Behav Ecol Sociobiol 63:627–636

    Google Scholar 

  54. Robinson EJH, Feinerman O, Franks NR (2012) Experience, corpulence and decision making in ant foraging. J Exp Biol 215:2653–2659

    PubMed  Google Scholar 

  55. Rueppell O, Kirkman RW (2005) Extraordinary starvation resistance in Temnothorax rugatulus (Hymenoptera, Formicidae) colonies: demography and adaptive behavior. Insect Soc 52:282–290

    CAS  Google Scholar 

  56. Scharf I (2016) The multifaceted effects of starvation on arthropod behaviour. Anim Behav 119:37–48

    Google Scholar 

  57. Schneirla TC (1971) Army ants: a study in social organization. W.H.Freeman & Co Ltd, Oxford

  58. Schultner E, Oettler J, Helanterä H (2017) The role of brood in eusocial Hymenoptera. Q Rev Biol 92:39–78

    PubMed  Google Scholar 

  59. Shaffer Z (2014) The wisdom of the acorn: social foraging in Temnothorax ants. Dissertation, Arizona State University

  60. Silberman RE, Gordon D, Ingram KK (2016) Nutrient stores predict task behaviors in diverse ant species. Insect Soc 63:299–307

    Google Scholar 

  61. Sternson SM, Nicholas Betley J, Cao ZFH (2013) Neural circuits and motivational processes for hunger. Curr Opin Neurobiol 23:353–360

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Teseo S, Delloro F (2017) Reduced foraging investment as an adaptation to patchy food sources: a phasic army ant simulation. J Theor Biol 428:48–55

    PubMed  Google Scholar 

  63. Toates FM (1986) Motivational systems (Problems in the Behavioural Sciences). Cambridge University Press, Cambridge

  64. Toth AL, Robinson GE (2005) Worker nutrition and division of labour in honeybees. Anim Behav 69:427–435

    Google Scholar 

  65. Toth AL, Kantarovich S, Meisel AF et al (2005) Nutritional status influences socially regulated foraging ontogeny in honey bees. J Exp Biol 208:4641–4649

    PubMed  Google Scholar 

  66. Traniello JFA (1977) Recruitment behavior, orientation, and the organization of foraging in the carpenter ant Camponotus pennsylvanicus degeer (Hymenoptera: Formicidae). Behav Ecol Sociobiol 2:61–79

    Google Scholar 

  67. Trible W, Olivos-Cisneros L, McKenzie SK et al (2017) orco mutagenesis causes loss of antennal lobe glomeruli and impaired social behavior in ants. Cell 170:727–735

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Ulrich Y, Burns D, Libbrecht R, Kronauer DJC (2016) Ant larvae regulate worker foraging behavior and ovarian activity in a dose-dependent manner. Behav Ecol Sociobiol 70:1011–1018

    PubMed  Google Scholar 

  69. Ulrich Y, Saragosti J, Tokita CK, Tarnita CE, Kronauer DJC (2018) Fitness benefits and emergent division of labour at the onset of group living. Nature 560:635–638

    CAS  PubMed  PubMed Central  Google Scholar 

  70. von Thienen W, Metzler D (2016) How memory and motivation modulate the responses to trail pheromones in three ant species. Behav Ecol Sociobiol 70:393–407

    Google Scholar 

  71. Vowles DM (1955) The foraging of ants. Br J Anim Behav 3:1–13

    Google Scholar 

  72. Wallis DI (1962) The relation between hunger, activity, and worker function in an ant colony. J Zool 139:589–605

    Google Scholar 

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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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Correspondence to Vikram Chandra or 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