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

  • Deby L. Cassill
  • Skye Brown
  • Devon Swick
  • George Yanev
Article

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.

Keywords

Wake/sleep cycles circadian rhythms 

Notes

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.

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 81–94Google 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 21:1–9Google Scholar
  3. Campbell SS, Tobler I (1984) Animal sleep: a review of sleep duration across phylogeny. Neuroscien Biobehav Rev 8:269–300CrossRefGoogle Scholar
  4. Cassill DL (2002) Yoyo-bang: a risk-aversion investment strategy by a perennial insect society. Oecologia 132:150–158CrossRefGoogle Scholar
  5. Cassill DL (2006) Why skew selection, a model of parental exploitation, should replace kin selection. J Bioecon 8:101–119CrossRefGoogle 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 50:801–813CrossRefGoogle 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 69–81Google Scholar
  8. Cassill DL, Tschinkel WR, Vinson SB (2002) Nest complexity, group size and brood rearing in the fire ant, Solenopsis invicta. Insectes Soc 49:158–163CrossRefGoogle Scholar
  9. Cirelli C, Bushey D, Hill S, Huber R, Kreber R, Ganetzky B, Tononi G (2005) Reduced sleep in Drosophila shaker mutants. Nature 434:1087–1092PubMedCrossRefGoogle Scholar
  10. Ghiselin M (1974) The economy of nature and the evolution of sex. University of California Press, Berkeley CA, USAGoogle Scholar
  11. Greenspan RJ, Tononi G, Cirelli C, Shaw P (2001) Sleep and the fruit fly. Trends Neuroscien 24:142–145CrossRefGoogle Scholar
  12. Griffith LC, Rosbash M (2008) Sleep: hitting the reset button. Nature Neuroscien 11:123–124CrossRefGoogle Scholar
  13. Hendricks JC, Sehgal A (2004) Why a fly? Using Drosophila to understand the genetics of circadian rhythms and sleep. Sleep 27:334–342PubMedGoogle 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 25:129–138PubMedCrossRefGoogle Scholar
  15. Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Ann Rev Neuroscien 20:595–631CrossRefGoogle Scholar
  16. Hobson JA (2005) Sleep is of the brain, by the brain and for the brain. Nature 437:1254–1256PubMedCrossRefGoogle Scholar
  17. Hölldobler B, Wilson EO (1990) The ants. Belknap Press of Harvard University Press, Cambridge Mass, USAGoogle Scholar
  18. Huber R, Ghilardi MF, Massimini M, Tononi G (2004) Local sleep and learning. Nature 430:78–81PubMedCrossRefGoogle 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 50:737–741CrossRefGoogle Scholar
  20. Kaiser W (2004) Busy bees need rest, too. J Compar Physiol A 163:565–584CrossRefGoogle Scholar
  21. Lima SL, Rattenborg NC, Lesku JA, Amlaner CJ (2005) Sleeping under the risk of predation. Anim Behav 70:723–736CrossRefGoogle Scholar
  22. Nitz DA, van Swinderen B, Tononi G, Greenspan RJ (2002) Electrophysiological correlates of rest and activity in Drosophila melanogaster. 12:1934–1940Google Scholar
  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 23:779–793CrossRefGoogle 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 15:395–402PubMedCrossRefGoogle 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, USAGoogle Scholar
  26. Shaw P (2003) Awakening to the behavioral analysis of sleep in Drosophila. J Biol Rhythms 18:4–11PubMedCrossRefGoogle Scholar
  27. Shaw PJ, Cirelli C, Greenspan RJ, Tononi G (2000) Correlates of sleep and waking in Drosophila melanogaster. Science 287:1834–1837PubMedCrossRefGoogle Scholar
  28. Stickgold R (2005) Insight review: sleep-dependent memory consolidation. Nature 437:1272–1278PubMedCrossRefGoogle Scholar
  29. Tietzel AJ, Lack LC (2002) The recuperative value of brief and ultra-brief naps on alertness and cognitive performance. J Sleep Research 11:213–218CrossRefGoogle Scholar
  30. Tobler I (1983) The effect of forced locomotion on the rest–activity cycle of the cockroach. Behav Brain Res 8:351–360PubMedCrossRefGoogle 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 9–30Google Scholar
  32. Tobler I, Borbély AA (1985) Effect of rest deprivation on motor activity of fish. J Comp Physiol A 157:817–822PubMedCrossRefGoogle Scholar
  33. Tobler I, Stalder J (1987) Rest in the scorpion—a sleep-like state? J Comp Physiol A 13:227–235Google 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 97:6914–6919CrossRefGoogle Scholar
  35. Tschinkel WR (1988) Social control of egg-laying rate in queens of the fire ant, Solenopsis invicta. Physiol Entomol 13:327–350CrossRefGoogle Scholar
  36. Tschinkel WR (2006) The fire ants. Harvard University Press, Cambridge, MA, p 669Google Scholar
  37. van Swinderen B, Nitz DA, Greenspan RJ (2004) Uncoupling of brain activity from movement defines arousal states in Drosophila. Current Biol 14:81–87Google 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 11:200–208CrossRefGoogle 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 5:2379–2397Google Scholar
  40. Zhdanova IV (2006) Sleep in zebrafish. Zebrafish 3:215–226PubMedCrossRefGoogle 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 27:337–350PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Deby L. Cassill
    • 1
  • Skye Brown
    • 2
  • Devon Swick
    • 2
  • George Yanev
    • 3
  1. 1.BiologyUSF St. PetersburgSt. PetersburgUSA
  2. 2.USFTampaUSA
  3. 3.MathematicsUniversity of TexasArlingtonUSA

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