Mapping sleeping bees within their nest: Spatial and temporal analysis of worker honey bee sleep

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Klein, Barrett Anthony ^a   Stiegler, Martin ^b   Klein, Arno ^c   Tautz, Jürgen ^b  

^a UNIVERSITY OF WISCONSIN LA CROSSE   (United States)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c SAGE BIONETWORKS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; APIS MELLIFERA; ARTICLE; BODY TEMPERATURE; BROOD PARASITE; CONTROLLED STUDY; ENVIRONMENTAL TEMPERATURE; FORAGER; HONEYBEE; INSECT CASTE; NONHUMAN; ORGANISM COLONY; SLEEP PATTERN; SPATIOTEMPORAL ANALYSIS; THERMOGRAPHY; WORKER (INSECT); AGE; ANIMAL; BEE; INFRARED RADIATION; NESTING; PHYSIOLOGY; SLEEP; SOCIAL DOMINANCE; SPATIAL BEHAVIOR; STATISTICAL MODEL; TEMPERATURE; TIME;

AGE FACTORS; ANIMALS; BEES; BODY TEMPERATURE; HIERARCHY, SOCIAL; INFRARED RAYS; LINEAR MODELS; NESTING BEHAVIOR; SLEEP; SPATIAL BEHAVIOR; TEMPERATURE; TIME FACTORS;

EID: 84904293319     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0102316     Document Type: Article

References (54)

1. Hay SI, Guerra CA, Gething PW, Patil AP, Tatem AJ, et al. (2009) A world malaria map: Plasmodium falciparum endemicity in 2007. PLoS Medicine 6: 286-302.
2. Witteveen BH, Worthy GAJ, Roth JD (2009) Tracing migratory movements of breeding North Pacific humpback whales using stable isotope analysis. Marine Ecology-Progress Series 393: 173-183.
3. Noser R, Byrne RW (2010) How do wild baboons (Papio ursinus) plan their routes? Travel among multiple high-quality food sources with inter-group competition. Anim Cogn 13: 145-155.
4. Jandt JM, Dornhaus A (2009) Spatial organization and division of labour in the bumblebee Bombus impatiens. Anim Behav 77: 641-651.
5. Franks NR, Sendova-Franks AB (1992) Brood sorting by ants: distributing the workload over the work-surface. Behav Ecol Sociobiol 30: 109-123. (Pubitemid 23400646)
6. Baracchi D, Zaccaroni M, Cervo R, Turillazzi S (2010) Home range analysis in the study of spatial organization on the comb in the paper wasp Polistes dominulus. Ethology 116: 579-587.
7. Adams ES, Tschinkel WR (1995) Spatial dynamics of colony interactions in young populations of the fire ant Solenopsis invicta. Oecologia 102: 156-163.
8. Menzel R, Greggers U, Smith A, Berger S, Brandt R, et al. (2005) Honey bees navigate according to a map-like spatial memory. P Natl Acad Sci USA 102: 3040-3045. (Pubitemid 40299912)
9. Riley JR, Greggers U, Smith AD, Reynolds DR, Menzel R (2005) The flight paths of honeybees recruited by the waggle dance. Nature. 435: 205-207. (Pubitemid 40685945)
10. Cartwright BA, Collett TS (1987) Landmark maps for honeybees. Biol Cybern 57: 85-93.
11. von Frisch K (1967) The Dance Language and Orientation of Bees. Cambridge: The Belknap Press.
12. Camazine S (1991) Self-Organizing Pattern Formation on the Combs of Honey Bee Colonies. Behav Ecol Sociobiol 28: 61-76.
13. Seeley TD (1982) Adaptive significance of the age polyethism schedule in honeybee colonies. Behav Ecol Sociobiol 11: 287-293.
14. Hendricks JC, Finn SM, Panckeri KA, Chavkin J, Williams JA, et al. (2000) Rest in Drosophila is a sleep-like state. Neuron 25: 129-138. (Pubitemid 30316516)
15. Anderson JR (1998) Sleep, sleeping sites, and sleep-related activities: awakening to their significance. Am J Primatol 46: 63-75.
16. Rattenborg NC, Lima SL, Amlaner CJ (1999) Half-awake to the risk of predation. Nature. 397: 397-398. (Pubitemid 129638165)
17. Anderson JR (2000) Sleep-related behavioural adaptations in free-ranging anthropoid primates. Sleep Med Rev 4: 355-373.
18. Piéron H (1913) Le Problème Physiologique du Sommeil. Paris: Masson.
19. Flanigan WF, Wilcox RH, Rechtschaffen A (1973) The EEG and behavioral continuum of the crocodilian, Caimen sclerops. Electroencephalogr Clin Neurophysiol 34: 521-538.
20. Tobler I (1985) Deprivation of sleep and rest in vertebrates and invertebrates. In: Inoue S, Borbely AA, editors. Endogenous Sleep Substances and Sleep Regulation (Taniguchi Symposia, series no. 8). Utrecht: VNU Science Press. pp. 57-66.
21. Kaiser W (1988) Busy bees need rest, too: Behavioural and electromyographical sleep signs in honeybees. J Comp Physiol A 163: 565-584.
22. Sauer S, Herrmann E, Kaiser W (2004) Sleep deprivation in honey bees. J Sleep Res 13: 145-152. (Pubitemid 38829895)
23. Seeley TD, Kolmes SA (1991) Age polyethism for hive duties in honey bees - illusion or reality? Ethology 87: 284-297.
24. Moore D, Angel JE, Cheeseman IM, Fahrbach SE, Robinson GE (1998) Timekeeping in the honey bee colony: integration of circadian rhythms and division of labor. Behav Ecol Sociobiol 43: 147-160. (Pubitemid 28395474)
25. Moore D (2001) Honey bee circadian clocks: behavioral control from individual workers to whole-colony rhythms. J Insect Physiol 47: 843-857.
26. Johnson BR (2008) With-in nest temporal polyethism in the honey bee. Behav Ecol Sociobiol 62: 777-784.
27. Klein BA, Olzsowy KM, Klein A, Saunders KM, Seeley TD (2008) Caste-dependent sleep of worker honey bees. J Exper Biol 211: 3028-3040. doi:10.1242/jeb.017426
28. Kleinhenz M, Bujok B, Fuchs S, Tautz J (2003) Hot bees in empty broodnest cells: heating from within. J Exp Biol 206: 4217-4231. (Pubitemid 38024786)
29. Kaiser W, Faltin T, Bayer G (2002) Sleep in a temperature gradient-behavioural recordings from forager honey bees. J Sleep Res 11 (suppl.): 115-116.
30. Schmolz E, Hoffmeister D, Lamprecht I (2002) Calorimetric investigations on metabolic rates and thermoregulation of sleeping honeybees (Apis mellifera carnica). Thermochim Acta 383: 221-227.
31. Seeley TD (1995) The Wisdom of the Hive: The Social Physiology of Honey Bee Colonies. Cambridge: Harvard University Press.
32. von Frisch K, Lindauer M, Inst Wiss Film (1977) Nachweis des Farbensehens bei der Honigbiene. Film C 1263 des IWF, Göttingen. Publication of Lindauer M, Publ Wiss Film, Sekt Biol, Ser. 14: Nr. 23/C 1263 (1981), 8 S.
33. Dustmann JH, Geffcken H (2000) Bienen können Farben unterscheiden. Nieders. Landesinstitut für Bienenkunde (Verleger), Celle.
34. Sakagami SF (1953) Untersuchungen über die Arbeitsteilung in einem Zwergvolk der Honigbiene. Beiträge zur Biologie des Bienenvolkes, Apis mellifera L. I. Jpn J Zool 11: 117-185.
35. Seeley TD (1985) Honeybee Ecology: A Study of Adaptation in Social Life. Princeton: Princeton University Press.
36. Kovac H, Stabentheiner A, Hetz SK, Petz M, Crailsheim K (2007) Respiration of resting honeybees. J Insect Physiol 53: 1250-1261. (Pubitemid 47633590)
37. Klein BA, Klein A, Wray MK, Mueller UG, Seeley TD (2010) Sleep Deprivation impairs precision of waggle dance signaling in honey bees. P Natl Acad Sci USA 107: 22705-22709. doi:10.1073/pnas.1009439108
38. Klein BA, Seeley TD (2011) Work or sleep? Honeybee foragers opportunistically nap during the day when forage is not available. Anim Behav 82: 77-83. doi:10.1016/j.anbehav.2011.03.026
39. R Development Core Team (2005) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. isbn 3-900051-07-0, online.
40. Bates D, Sarkar D (2006) The lme4 Package, http://cran.r-project.org/src/ contrib/Descriptions/lme4.html.
41. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical J 50: 346-363.
42. Pinheiro J, Bates D (2002) Mixed-Effects Models in S and S-PLUS. New York: Springer. pp. 83-92.
43. Clark DL, Gillingham JC (1990) Sleep-site fidelity in two Puerto Rican lizards. Anim Behav 39: 1138-1148. (Pubitemid 20429333)
44. Bujok B, Kleinhenz M, Fuchs S, Tautz J (2002) Hot spots in the bee hive. Naturwissenschaften 89: 299-301. (Pubitemid 34827945)
45. Vega L, Torres A, Hoffmann W, Lamprecht I (2011) Thermal investigations associated with the behaviour patterns of resting workers of Bombus atratus (Hymenoptera: Apidae). J Therm Anal Calorim 104: 233-237.
46. Hess WR (1926) Die Temperaturregulierung im Bienenvolk. Z Vergl Physiol 4: 465-487.
47. Szabo TI (1985) The thermology of wintering honeybee colonies in 4-colony packs as affected by various hive entrances. J Apicultural Res 24: 27-37.
48. Humphrey JAC, Dykes ES (2008) Thermal energy conduction in a honey bee comb due to cell-heating bees. J Theor Biol 250: 194-208. (Pubitemid 350160715)
49. Fahrenholz L, Lamprecht I, Schricker B (1989) Thermal investigations of a honey bee colony: thermoregulation of the hive during summer and winter and heat production of members of different bee castes. J Comp Physiol B 159: 551-560.
50. Stabentheiner A, Kovac H, Brodschneider R (2010) Honeybee colony thermoregulation - regulatory mechanisms and contribution of individuals in dependence on age, location and thermal stress. PLoS One 5: 1-13.
51. Sauer S, Kinkelin M, Herrmann E, Kaiser W (2003) The dynamics of sleep-like behaviour in honey bees. J Comp Physiol A 189: 599-607. (Pubitemid 37105901)
52. Sauer S, Menna-Barreto L, Kaiser W (1998) The temporal organization of rest and activity in newly emerged honey bees kept in isolation - initial results. Apidologie 29: 445-447.
53. Sauer S, Happel U, Neubecker R, Menna-Barreto L, Herrmann E, Kaiser W (1999) Ontogeny of the circadian rest-activity cycle in honey bees kept in isolation. In: Elsner N, Eysel U. Proceedings of the 1st Göttingen Conference of the German Neuroscience Society, vol. II: 27th Göttingen Neurobiology Conference. Stuttgart: Georg Thieme Verlag. p. 241.
54. Eban-Rothschild AD, Bloch G (2008) Differences in the sleep architecture of forager and young honeybees (Apis mellifera). J Exper Biol 211: 2408-2416.