Abstract
At night, honey bees pass through a physiological state that is similar to mammalian sleep. Like sleep in mammals, sleep-like behaviour in honey bees is an active process. This is expressed most clearly in these insects by spontaneous antennal movements which appear at irregular intervals throughout the night and interrupt episodes of antennal immobility. Here we present a newly developed video technique for the continuous recording of the position and movements of the bee's antennae. The same technique was used to record head inclination and ventilatory movements. Despite the constancy of the ambient temperature, the magnitudes of antennae-related parameters, as well as head inclination and ventilatory cycle duration, displayed dynamic unimodal time-courses which exhibited a high degree of temporal covariance. The similarity between these time-courses and the nightly time-course of the reaction threshold for a sensory stimulus, investigated previously, indicates that, in honey bees, deepest "sleep" and least ventilatory activity occur at the same time (in the 7th hour of the rest phase).
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Abbreviations
- DD:
-
continuous darkness
- EMG:
-
electromyogram
- LD:
-
periodic alternation between light (L) and darkness (D)
- MEST:
-
Middle European Summer Time (UTC+2 h);
- UV:
-
ultraviolet
References
Andersen FO (1968) Sleep in moths and its dependence on the frequency of stimulation in Anagasta kuehniella. Opusc Entomol 33:15–24
Crailsheim K, Eggenreich U, Ressi R, Szolderits MJ (1999) Temperature preference of honeybee drones (Hymenoptera: Apidae). Entomol Gener 24:37–47
Erber J, Pribbenow B, Kisch J, Faensen D (2000) Operant conditioning of antennal muscle activity in the honey bee (Apis mellifera L.). J Comp Physiol A 186:557–565
Grziwa J (1961) Arbeiten die Bienen auch nachts? Imkerfreund 16:161–163
Harris JW, Woodring J (1992) Effects of stress, age, season, and source colony on levels of octopamine, dopamine and serotonin in the honey bee (Apis mellifera L.) brain. J Insect Physiol 38:29–35
Haufe WO (1963) Ethological and statistical aspects of a quantal response in mosquitoes to environmental stimuli. Behaviour 20:221–241
Hendricks JC, Finn SM, Panckeri KA, Chavkin J, Williams JA, Sehgal A, Pack AI (2000) Rest in Drosophila is a sleep-like state. Neuron 25:129–138
Hess WR (1926) Die Temperaturregulierung im Bienenvolk. Z Vergl Physiol 4:465–487
Hobson JA (1989) Sleep. Scientific American Library, a Division of HPHLP, New York, USA
Hoffmann RW (1937) Der Insektenschlaf als reflektorische Immobilisation. Naturwissenschaften 25:359–366
Kaiser W (1983) Effects of non-visual and circadian inputs to visual interneurones in the honey bee. In: Horn E (ed) Fortschritte der Zoologie 28: multimodal convergences in sensory systems. Fischer, Stuttgart, pp 149–166
Kaiser W (1988) Busy bees need rest, too. Behavioural and electromyographical sleep signs in honeybees. J Comp Physiol A 163:565–584
Kaiser W (1995) Rest at night in some solitary bees—a comparison with the sleep-like state of honey bees. Apidologie 26:213–230
Kaiser W (2000) Sleep in insects. World Fed Sleep Res Soc Newsletter Online 8, issue 1. http://www.wfsrs.org/newsletters/Newsletter8_1/inside/images.html
Kaiser W (2002) Honey bee sleep is different from chill coma—behavioural and electrophysiological recordings in forager honey bees. J Sleep Res 11 [Suppl 1]:115
Kaiser W, Jander JP (1988) Electromyographic indicators of sleep and wakefulness of honey bees. In: Koella WP, Obál F, Schulz H, Visser P (eds) Sleep 86 (Proc 8th Eur Cong Sleep Res). Fischer, Stuttgart, pp 249–251
Kaiser W, Steiner-Kaiser J (1983) Neuronal correlates of sleep, wakefulness and arousal in a diurnal insect. Nature 301:707–709
Kaiser W, Weber T, Otto D (1996) Vegetative physiology at night in honey bees. In: Elsner N, Schnitzler HU (eds) Brain and evolution. Proc 24th Göttingen Neurobiol Conf, vol II. Thieme, Stuttgart, pp 140
Lindauer M (1952) Ein Beitrag zur Frage der Arbeitsteilung im Bienenstaat. Z Vergl Physiol 34:299–345
Livingstone MS, Hubel DH (1981) Effects of sleep and arousal on the processing of visual information in the cat. Nature 291:554–561
Martin H, Lindauer M (1966) Sinnesphysiologische Leistungen beim Wabenbau der Honigbiene. Z Vergl Physiol 53:372–404
Mill PJ (1985) Integument, respiration and circulation. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology biochemistry and pharmacology, vol 3. Pergamon Press, Oxford, pp 546–564
Rattenborg NC, Amlaner CJ (2002) Phylogeny of sleep. In: Lee-Chiong TL, Sateia MJ, Carskadon MA (eds) Sleep medicine. Hanley & Belfus, Philadelphia, pp 7–22
Sauer S, Kaiser W (1995) Pollen foragers of the honey bee (Apis mellifera carnica L) rest in the hive at night. In: Elsner N, Menzel R (eds) Learning and memory. Proc 23rd Göttingen Neurobiol Conf. Thieme, Stuttgart, pp 253
Sauer S, Kaiser W (1996a) Sleep-like behaviour of honey bees follows a circadian rhythm. Verh Dtsch Zool Ges 89:292
Sauer S, Kaiser W (1996b) The nocturnal behaviour of pollen forager honey bees (Apis mellifera carnica L) in an observation hive. Apidologie 27:317–318
Sauer S, Kaiser W, Sauer M (1997a) The microstructure of sleep in honey bees—a statistical analysis of antennal immobility. Verh Dtsch Zool Ges 90:316
Sauer S, Kinkelin M, Kaiser W (1997b) Sleep in honey bees is a dynamic process. Apidologie 28:213–215
Sauer S, Herrmann E, Kaiser W (1998a) The temporal occurrence of antennal motility during sleep in honey bees can be described by a non-stationary Poisson process. In: Elsner N, Wehner R (eds) New neuroethology on the move. Proc 26th Göttingen Neurobiol Conf, vol II. Thieme, Stuttgart, pp 266
Sauer S, Herrmann E, Kaiser W (1998b) Covariation of behavioural sleep signs and resting respiration in honey bees. J Sleep Res 7 [Suppl 2]:240
Sauer S, Kinkelin M, Kaiser W (1998c) Measurement of behavioral sleep signs in honeybees with a custom designed video interface. In: Noldus LPJJ (ed) Measuring behavior 98. Proceedings of the 2nd International Conference on Methods and Techniques in Behavioural Research. Noldus Information Technology, Wageningen Netherlands, pp 249–250 (http://www.noldus.com/events/mb98/abstracts/sauer.htm)
Schuppe H, Burrows M (1996a) Characterization of resting states in locusts. Verh Dtsch Zool Ges 89:296
Schuppe H, Burrows M (1996b) Palp movements in resting locusts. In: Elsner N, Schnitzler HU (eds) Brain and evolution. Proc 24th Göttingen Neurobiol Conf, vol II. Thieme, Stuttgart New York, pp 119
Shaw PJ, Cirelli C, Greenspan RJ, Tononi G (2000) Correlates of sleep and waking in Drosophila melanogaster. Science 287:1834–1837
Szymczak JT (1987) Daily distribution of sleep states in the rook Corvus frugilegus. J Comp Physiol A 161:321–327
Tobler I (1983) Effect of forced locomotion on the rest-activity cycle of the cockroach. Behav Brain Res 8:351–360
Tobler I (1984) Evolution of the sleep process: a phylogenetic approach. In: Borbély AA, Valatx JL (eds) Sleep mechanisms. Exp Brain Res [Suppl 8]. Springer, Berlin Heidelberg New York, pp 207–226
Tobler I (2000) Phylogeny of sleep regulation. In: Kryger MH, Roth T, Dement WC (eds) Principles and practice of sleep medicine, 3rd edn. Saunders, Philadelphia, pp 72–81
Tobler I, Neuner-Jehle M (1992) 24-h variation of vigilance in the cockroach Blaberus giganteus. J Sleep Res 1:231–239
Tobler I, Stalder J (1988) Rest in the scorpion—a sleep-like state? J Comp Physiol A 163:227–235
Zepelin H (2000) Mammalian sleep. In: Kryger MH, Roth T, Dement WC (eds) Principles and practice of sleep medicine, 3rd edn. Saunders, Philadelphia, pp 82–92
Acknowledgements
Our special thanks go to Prof. Dr.-Ing. Dr. hc. Willmut Zschunke and Heinz Helmuth Grimm (Department of Electrical Engineering and Information Technology, Darmstadt University of Technology) for the development and construction of the video interface. Theo Zaschka (München) produced the excellent, custom-built mechanical parts of the experimental apparatus. We thank Gabriele Bayer for her technical assistance and Jana Steiner-Kaiser for the translation of the manuscript and numerous helpful and critical discussions. We are grateful to the Deutsche Forschungsgemeinschaft for funding the experimental setup under the programme SFB 45 "Comparative Neurobiology of Behaviour".
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This paper is dedicated to Professor Martin Lindauer, who—to our knowledge—was the first to meticulously record the nightly behaviour of honey bees (Lindauer 1952) and who also inspired one of us (W.K.) to investigate antennal motility during nightly rest in these animals.
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Sauer, S., Kinkelin, M., Herrmann, E. et al. The dynamics of sleep-like behaviour in honey bees. J Comp Physiol A 189, 599–607 (2003). https://doi.org/10.1007/s00359-003-0436-9
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DOI: https://doi.org/10.1007/s00359-003-0436-9