Polyphasic Wake/Sleep Episodes in the Fire Ant, Solenopsis Invicta

Abstract

Sleep is a well-studied biological process in vertebrates, particularly birds and mammals. Less is know about sleep in solitary and social invertebrates, particularly the ants. This paper reports a study of light/dark periods on worker activity as well as sleep location, posture and the wake/sleep cycles of fire ant workers and queens located in an artificial nest chamber. Workers slept in one of three locations: on the ceiling, against the chamber wall or in the center of the chamber floor. Workers on the ceiling or against the chamber wall slept for longer periods than those at the center of the chamber floor where most grooming and feeding activity occurred. When sleeping, queens huddled together. Their close contact generated synchronized wake/sleep cycles with each other. Sleep posture was distinctly different than wake posture. During deep sleep, queens and workers folded their antennae and were non-responsive to contact by other ants. Another indicator of deep sleep was rapid antennal movement (RAM sleep). Sleep episodes were polyphasic. Queens averaged ~92 sleep episodes per day, each episode lasting ~6 min, for a total of ~9.4 h of sleep per day. Workers averaged ~253 sleep episodes lasting 1.1 min each for a total of ~4.8 h of sleep per day. Activity episodes were unaffected by light/dark periods. Workers were hypervigilant with an average of 80% of the labor force completing grooming, feeding or excavation tasks at any given time. These findings reinforce the parental exploitation hypothesis—sterile workers are a caste of disposable, short-lived helpers whose vigilance and hyperactivty increases the queen’s fitness by buffering her and her fertile offspring from environmental stresses.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Amlaner CL, Ball NJ (1994) Avian sleep. In: Kryger MH, Roth T, Dement WC (eds) Principles and practice of sleep medicine, 2nd edn. WB Saunders, Philadelphia, pp 81–94

    Google Scholar 

  2. Banks WA, Lofgren CS, Jouvenez DP, Stringer CE, Bishop PM, Williams DF, Wojcik DP, Glancey BM (1981) Techniques for rearing, collecting and handling imported fire ants. USDA and SEA Agric Technol Southern Ser 21:1–9

    Google Scholar 

  3. Campbell SS, Tobler I (1984) Animal sleep: a review of sleep duration across phylogeny. Neuroscien Biobehav Rev 8:269–300

    Article  CAS  Google Scholar 

  4. Cassill DL (2002) Yoyo-bang: a risk-aversion investment strategy by a perennial insect society. Oecologia 132:150–158

    Article  Google Scholar 

  5. Cassill DL (2006) Why skew selection, a model of parental exploitation, should replace kin selection. J Bioecon 8:101–119

    Article  Google Scholar 

  6. 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

    Article  Google Scholar 

  7. Cassill DL, Tschinkel WR (1999) Information flow during social feeding in ant societies. In: Detrain CT, Pasteels JL (eds) Information processing in social insects. Birkauser Verlag, Basel, Switzerland, pp 69–81

    Google Scholar 

  8. Cassill DL, Tschinkel WR, Vinson SB (2002) Nest complexity, group size and brood rearing in the fire ant, Solenopsis invicta. Insectes Soc 49:158–163

    Article  Google Scholar 

  9. Cirelli C, Bushey D, Hill S, Huber R, Kreber R, Ganetzky B, Tononi G (2005) Reduced sleep in Drosophila shaker mutants. Nature 434:1087–1092

    PubMed  Article  CAS  Google Scholar 

  10. Ghiselin M (1974) The economy of nature and the evolution of sex. University of California Press, Berkeley CA, USA

    Google Scholar 

  11. Greenspan RJ, Tononi G, Cirelli C, Shaw P (2001) Sleep and the fruit fly. Trends Neuroscien 24:142–145

    Article  CAS  Google Scholar 

  12. Griffith LC, Rosbash M (2008) Sleep: hitting the reset button. Nature Neuroscien 11:123–124

    Article  CAS  Google Scholar 

  13. Hendricks JC, Sehgal A (2004) Why a fly? Using Drosophila to understand the genetics of circadian rhythms and sleep. Sleep 27:334–342

    PubMed  Google Scholar 

  14. Hendricks JC, Finn SM, Panckeri KA, Chavkin J, Williams JA, Sehgal A, Pack AL (2000) Rest in Drosophila is a sleep-like state. Neuron 25:129–138

    PubMed  Article  CAS  Google Scholar 

  15. Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Ann Rev Neuroscien 20:595–631

    Article  CAS  Google Scholar 

  16. Hobson JA (2005) Sleep is of the brain, by the brain and for the brain. Nature 437:1254–1256

    PubMed  Article  CAS  Google Scholar 

  17. Hölldobler B, Wilson EO (1990) The ants. Belknap Press of Harvard University Press, Cambridge Mass, USA

    Google Scholar 

  18. Huber R, Ghilardi MF, Massimini M, Tononi G (2004) Local sleep and learning. Nature 430:78–81

    PubMed  Article  CAS  Google Scholar 

  19. Ishay JS, Pertsis V, Levtov E (2005) Duration of hornet sleep induced by ether anesthesia in curtailed by exposure to sun or UV irradiation. Cell Mol Life Scien 50:737–741

    Article  Google Scholar 

  20. Kaiser W (2004) Busy bees need rest, too. J Compar Physiol A 163:565–584

    Article  Google Scholar 

  21. Lima SL, Rattenborg NC, Lesku JA, Amlaner CJ (2005) Sleeping under the risk of predation. Anim Behav 70:723–736

    Article  Google Scholar 

  22. Nitz DA, van Swinderen B, Tononi G, Greenspan RJ (2002) Electrophysiological correlates of rest and activity in Drosophila melanogaster. 12:1934–1940

  23. Paredes SD, Cubero J, Valero V, Barriga C, Reiter RJ, Rodriguez AB (2006) Comparative study of the activity/rest rhythms in young and old ringdove (Streptopelia Risoria): correlation with serum levels of melatonin and serotonin. Chronobiol Intern 23:779–793

    Article  CAS  Google Scholar 

  24. Roth II TC, Lesku JA, Amlaner CJ, Lima SL (2006) A phylogenetic analysis of the correlates of sleep in birds. J Sleep Res 15:395–402

    PubMed  Article  Google Scholar 

  25. Sall J, Lehman A (2005) JMP start statistics: a guide to statistics and data analysis using JMP and JMP IN software. Duxbury Press, Albany, NY, USA

    Google Scholar 

  26. Shaw P (2003) Awakening to the behavioral analysis of sleep in Drosophila. J Biol Rhythms 18:4–11

    PubMed  Article  Google Scholar 

  27. Shaw PJ, Cirelli C, Greenspan RJ, Tononi G (2000) Correlates of sleep and waking in Drosophila melanogaster. Science 287:1834–1837

    PubMed  Article  CAS  Google Scholar 

  28. Stickgold R (2005) Insight review: sleep-dependent memory consolidation. Nature 437:1272–1278

    PubMed  Article  CAS  Google Scholar 

  29. Tietzel AJ, Lack LC (2002) The recuperative value of brief and ultra-brief naps on alertness and cognitive performance. J Sleep Research 11:213–218

    Article  Google Scholar 

  30. Tobler I (1983) The effect of forced locomotion on the rest–activity cycle of the cockroach. Behav Brain Res 8:351–360

    PubMed  Article  CAS  Google Scholar 

  31. Tobler I (1989) Sleep and alertness: Chronobiological, behavioral, and medical aspects of napping. In: Dinges DF, Broughton RJ (eds) Napping and polyphasic sleep in mammals. Raven, New York, pp 9–30

    Google Scholar 

  32. Tobler I, Borbély AA (1985) Effect of rest deprivation on motor activity of fish. J Comp Physiol A 157:817–822

    PubMed  Article  CAS  Google Scholar 

  33. Tobler I, Stalder J (1987) Rest in the scorpion—a sleep-like state? J Comp Physiol A 13:227–235

    Google Scholar 

  34. Toma DP, Bloch G, Moore D, Robinson GE (2000) Changes in period mRNA levels in the brain and division of labor in honey bee colonies. Proc Nat Acad Scien 97:6914–6919

    Article  CAS  Google Scholar 

  35. Tschinkel WR (1988) Social control of egg-laying rate in queens of the fire ant, Solenopsis invicta. Physiol Entomol 13:327–350

    Article  Google Scholar 

  36. Tschinkel WR (2006) The fire ants. Harvard University Press, Cambridge, MA, p 669

    Google Scholar 

  37. van Swinderen B, Nitz DA, Greenspan RJ (2004) Uncoupling of brain activity from movement defines arousal states in Drosophila. Current Biol 14:81–87

    Google Scholar 

  38. Vyazovskiy VV, Cirelli C, Pfister-Genskow M, Faraguna U, Tononi G (2008) Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nature Neuroscien 11:200–208

    Article  CAS  Google Scholar 

  39. Yokogawa T, Marin W, Faraco J, Pézeron G, Appelbaum L, Zhang J, Rosa F, Mourrain P, Mignot E (2007) Characterization of sleep in zebrafish and insomnia in hypocretin receptor mutants. PloS 5:2379–2397

    CAS  Google Scholar 

  40. Zhdanova IV (2006) Sleep in zebrafish. Zebrafish 3:215–226

    PubMed  Article  CAS  Google Scholar 

  41. Zimmerman JE, Rizzo W, Shockley KR, Raizen DM, Naidoo N, Mackiewicz M, Chrichill GA, Pack AI (2006) Multiple mechanisms limit the duration of wakefulness in Drosophila brain. Physiol Genomics 27:337–350

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank USF St. Petersburg undergraduates Kim Vo, Lieu Huynh and Thomas Watkins for recording data on individual workers. Lastly, we thank the editor, Thomas Payne, and three anonymous reviewers for critical improvements to the initial manuscript—very helpful. The work reported herein was funded in part by the Texas Fire Ant Research Initiative 1995–2005.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Deby L. Cassill.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Cassill, D.L., Brown, S., Swick, D. et al. Polyphasic Wake/Sleep Episodes in the Fire Ant, Solenopsis Invicta . J Insect Behav 22, 313 (2009). https://doi.org/10.1007/s10905-009-9173-4

Download citation

Keywords

  • Wake/sleep cycles
  • circadian rhythms