Respiratory rhythms in stingless bee workers: Circadian and ultradian components throughout adult development

Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology

Volumn 197, Issue 4, 2011, Pages 361-372

  Teixeira, Laura V ^a   Waterhouse, Jim M ^b   Marques, Mirian D ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b LIVERPOOL JOHN MOORES UNIVERSITY   (United Kingdom)

Author keywords

Circadian rhythms; Internal temporal order; Ontogeny; Stingless bees; Ultradian rhythms

Indexed keywords

AGING; ANALYSIS OF VARIANCE; ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BEE; BREATHING MECHANICS; CIRCADIAN RHYTHM; CLASSIFICATION; EXPLORATORY BEHAVIOR; FEMALE; GROWTH, DEVELOPMENT AND AGING; OXYGEN CONSUMPTION; PERIODICITY; PHYSIOLOGY; SEASON; SOCIAL BEHAVIOR;

ACTIVITY CYCLES; AGING; ANALYSIS OF VARIANCE; ANIMALS; BEES; BEHAVIOR, ANIMAL; CIRCADIAN RHYTHM; EXPLORATORY BEHAVIOR; FEMALE; OXYGEN CONSUMPTION; RESPIRATORY MECHANICS; SEASONS; SOCIAL BEHAVIOR;

EID: 79952992144     PISSN: 03407594     EISSN: 14321351     Source Type: Journal    
DOI: 10.1007/s00359-010-0620-7     Document Type: Article

References (53)

1. Alves DA, Menezes C, Imperatriz-Fonseca V, Wenseleers T (2010) First discovery of a rare polygyne colony in the stingless bee Melipona quadrifasciata (Apidae, Meliponini). Apidologie. doi: 10.1051/Apido/2010053.
2. Aschoff J (1960) Exogenous and endogenous components in circadian rhythms. Cold Spring Harb Symp Quant Biol 25: 11-28.
3. Bellusci S, Marques MD (2001) Circadian activity rhythm of the foragers of a eusocial bee (Scaptotrigona aff. depilis, Hymenoptera, Apidae, Meliponinae) outside the nest. Biol Rhythm Res 32: 117-124.
4. Bloch G, Robinson GE (2001) Reversal of honeybee behavioural rhythms. Nature 410: 1048.
5. Borges FB, Blochtein B (2006) Variação sazonal das condições internas de colônias de Melipona marginata obscurior Moure, no Rio Grande do Sul, Brasil. Rev Bras Zool 23: 711-715.
6. Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, Princeton.
7. Contel EPB, Kerr WE (1976) Origin of males in Melipona subnitida estimated from data of an isozymic polymorphic system. Genetica 46: 271-277.
8. Eban-Rothschild A, Bloch G (2008) Differences in the sleep architecture of forager and young honeybees (Apis mellifera). J Exp Biol 211: 2408-2416.
9. Engels W, Rosenkranz P, Engels E (1995) Thermoregulation in the nest of the neotropical stingless bee Scaptotrigona postica and a hypothesis on the evolution of the temperature homeostasis in highly eusocial bees. Stud Neotropical Fauna Environ 30: 193-205.
10. Frisch B, Koeniger N (1994) Social synchronization of the activity rhythms of honeybees within a colony. Behav Ecol Sociobiol 35: 91-98.
11. Gomes FR, Chaui-Berlinck JG, Bicudo JEPW, Navas CA (2004) Intraspecific relationships between resting and activity metabolism in anuran amphibians: influence of ecology and behavior. Physiol Biochem Zool 77: 197-208.
12. Hartfelder K, Makert GR, Judice CC, Pereira GAG, Santana WC, Dallacqua R, Bitondi MMG (2006) Physiological and genetic mechanisms underlying caste development, reproduction and division of labor in stingless bees. Apidologie 37: 144-163.
13. Kaiser W (1988) Busy bees need rest, too: behavioural and eletromyographic sleep signs in honeybees. J Comp Physiol 163: 565-584.
14. Kaiser W, Steiner-Kaiser J (1983) Neuronal correlates of sleep wakefulness and arousal in a diurnal insect. Nature 301: 707-709.
15. Kerr WE, dos Santos Neto GR (1956) Contribuição para o conhecimento da bionomia dos Meliponini. V. Divisão de trabalho entre operárias de M. quadrifasciata quadrifasciata Lep. Ins Soc 3: 423-430.
16. Kerr WE, Zucchi R, Nakadaira JT, Butolo JE (1962) Reproduction in the social bees (Hymenoptera: Apidae). J New York Entomol Soc 70: 265-276.
17. Kleinhenz M, Bujok B, Fuchs S, Tautz J (2003) Hot bees in empty brood nest cells: heating from within. J Exp Biol 206: 4217-4231.
18. Machado MFPS, Contel EPB, Kerr WE (1984) Proportion of males sons-of-the-queen and sons-of-workers in Plebeia droryana (Hymenoptera, Apidae) estimated from data of an MDH isozymic polymorphic system. Genetica 65: 193-198.
19. Macieira OJD, Proni EA (2005) Influência da temperatura na taxa respiratória de abelhas forrageiras Trigona spinipes (Fabricius) (Hymenoptera, Apidade, Meliponinae) durante períodos de verão e inverno. Rev Bras Zool 22: 1159-1163.
20. Maleska J, Barron AB, Helliwell PG, Maleska R (2009) Effect of age, behaviour and social environment on honey bee brain plasticity. J Comp Physiol A 195: 733-740.
21. Marques MD, Yamashita CE (2008) Biological rhythms in the colony of stingless bees. In: Fanjul-Moles ML, Aguilar-Roblero R (eds) Comparative aspects of circadian rhythms. Transworld Research Network, Kerala, pp 93-107.
22. Menzel R, Ventura DF, Werner A, Joaquim LCM, Backhaus W (1989) Spectral sensitivity of single photoreceptors and color vision in the stingless bee, Melipona quadrifasciata. J Comp Physiol A 166: 151-164.
23. Michener CD (1974) The social behavior of the bees. A comparative study. The Belknap Press of Harvard University Press, Cambridge.
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.
25. Moore-Ede MC, Sulzman FM (1981) Internal temporal order. In: Aschoff J (ed) Biological rhythms. Handbook of behavioral neurobiology, vol 4th. Plenum Press, New York, pp 215-241.
26. Moritz RFA, Sakofski F (1991) The role of the queen in circadian rhythms of honeybees (Apis mellifera L.). Behav Ecol Sociobiol 29: 361-365.
27. Moritz RFA, Southwick EE (1992) Bees as superorganisms: an evolutionary reality. Springer, Berlin.
28. Nelson W, Tong YL, Lee JK, Halberg F (1979) Methods for cosinor-rhythmometry. Chronobiologia 6: 305-323.
29. Nevill AM, Teixeira LV, Marques MD, Waterhouse JM (2004) Using covariance to unravel the effects of meteorological factors and daily and seasonal rhythms. Biol Rhythm Res 35: 159-169.
30. Oda GA, Bellusci S, Marques MD (2007) Daily rhythms related to distinct social tasks inside an eusocial bee colony. Chronobiol Int 24: 845-858.
31. Page TL (1989) Masking in invertebrates. Chronobiol Int 6: 3-11.
32. Paxton RJ, Weißschuh N, Engels W, Hartfelder K (1999) Not only single mating in stingless bees. Naturwissenschaften 86: 143-146.
33. Peters JM, Queller DC, Imperatriz-Fonseca VL, Roubik DW, Strassmann JE (1999) Mate number, kin selection and social conflicts in stingless bees and honeybees. Proc R Soc Lond B 266: 379-384.
34. Pittendrigh CS, Daan S (1976) A functional analysis of circadian pacemakers in nocturnal rodents. I. The stability and lability of spontaneous frequency. J Comp Physiol A 106: 223-252.
35. Proni EA, Macieira OJD (2004) Ritmo circadiano da taxa respiratória de Tetragonisca angustulafiebrigi (Schwarz), T. a. angustula (Latreille) e Trigona spinipes (Fabricius) (Hymenoptera, Apidae, Meliponinae). Rev Bras Zool 21: 987-993.
36. Regal PJ, Connolly MS (1980) Social influences on biological rhythms. Behaviour 72: 171-199.
37. Rothe U, Nachtigall W (1989) Flight of the honey bee. IV. Respiratory quotients and metabolic rates during sitting, walking and flying. J Comp Physiol B 158: 739-749.
38. Roubik DW, Peralta FJA (1983) Thermodynamics in nests of two Melipona species in Brasil. Acta Amazon 13: 453-466.
39. Sakagami SF (1982) Stingless bees. In: Hermann HR (ed) Social insects. Academic Press, New York, pp 361-423.
40. Sakagami SF, Zucchi R (1974) Oviposition behavior of two dwarf stingless bees, Hypotrigona (Leurotrigona) muelleri and H. (Trigonisca) duckei, with notes on the temporal articulation of oviposition process in stingless bees. J Fac Sci Hokkaido Univ VI Zool 1: 361-421.
41. Sakagami SF, Beig D, Akahira Y (1963) Occurrence of ovary developed workers in queen right colonies of stingless bees. Rev Brasil Biol 23: 115-129.
42. Sehgal A, Price J, Young MW (1992) Ontogeny of biological clock in Drosophila melanogaster. Proc Natl Acad Sci USA 89: 1423-1427.
43. Shemesh Y, Cohen M, Bloch G (2007) Natural plasticity in circadian rhythms is mediated by reorganization in the molecular clockwork in honeybees. FASEB J 21: 2304-2311.
44. Shemesh Y, Eban-Rothschild A, Cohen M, Bloch G (2010) Molecular dynamics and social regulation of context-dependent plasticity in the circadian clockwork of the honey bee. J Neurosci 30: 12517-12525.
45. Sommeijer MJ (1984) Distribution of labour among workers of Melipona favosa F.: age-polyethism and worker oviposition. Ins Soc 2: 171-184.
46. Stussi Th (1972) Ontogenèse du rythme circadien de la dépense énergétique chez l'abeille. Arch Sci Physiol 26: 161-173.
47. Takahashi-Del Bianco M, Benedito-Silva AA, Hebling MJA, Marques N, Marques MD (1992) Circadian oscillatory patterns of oxygen uptake in individual workers of the ant Camponotusrufipes. Physiol Entomol 17: 377-383.
48. Teixeira LV, Bellusci S, Oda GA, Almeida GF, Marques MD (2004) Rhythms in eusocial bee colonies (Frieseomelitta varia and F. doederleini, Tribe Meliponini). In: Proceedings of 8th international conference on tropical bees and VI Encontro sobre Abelhas, pp 731.
49. van Nerum K, Buelens H (1997) Hypoxia-controlled winter metabolism in honeybees (Apis mellifera). Comp Biochem Physiol A 117: 445-455.
50. Wille A (1983) Biology of the stingless bees. Ann Rev Entomol 28: 41-64.
51. Winfree AT (1967) Biological rhythms and the behavior of populations of coupled oscillators. J Theor Biol 16: 15-42.
52. Zucchi R (1993) Ritualized dominance, evolution of queen-worker interactions and related aspects in stingless bees (Hymenoptera: Apidae). In: Inoue T, Yamane S (eds) Evolution of insect societies. Hakuhiusha, Tokyo, pp 207-249.
53. Zucchi R, da Silva-Matos EV, Nogueira-Ferreira FH, Azevedo GG (1999) On the cell provisioning and oviposition process (POP) of the stingless bees-nomenclature reappraisal and evolutionary considerations (Hymenoptera, Apidae, Meliponinae). Sociobiology 34: 65-86.