The Same Photoperiodic Clock May Control Induction and Maintenance of Diapause in the Spider Mite Tetranchus urticae

Abstract

In the spider mite Tetranychus urticae, both diapause induction (which takes place during the larval and nymphal stages) and diapause maintenance (in the adult female) are under photoperiodic control. The question of whether or not the same photoperiodic clock is involved in both photoperiodic reactions was investigated in eight strains of the spider mite, originating from different localities in Europe. The methods employed consisted of (1) determination of the relative importance of the photophase and scotophase in the two photoperiodic reactions; (2) comparison of photoperiodic response curves for diapause induction and diapause maintenance; and (3) determination of the effect of light breaks on the capacity of long nights to maintain diapause, and comparison with the effect of light breaks in diapause induction experiments.

Keywords

photoperiodism diapause geographic strains spider mites Acarina Tetranychidae Tetranychus urticae

References

Adams, A.J. (1986) Night-interruption experiments and action spectra for dawn and dusk in relation to the photoperiodic clock of the cabbage whitefly, Aleyrodes proletella (Homoptera: Aleyrodidae. J. Insect Physiol. 32: 71-78.

Ankersmit, G.W. (1968) The photoperiod as a control agent against Adoxophyes reticulana (Lepidoptera; Tortricidae. Entomol. Exp. Appl. 11: 231-240.

Beach, R.F. , and G.B. Craig, JR. (1977) Night length measurements by the circadian clock controlling diapause induction in the mosquito Aedes atropalpus . J. Insect Physiol. 23: 865-870.

Beards, G.W. , and F.E. Strong (1966) Photoperiod in relation to diapause in Lygus hesperus Knight. Hilgardia 37: 345-362.

Bell, R.A. , C.G. Rasul , and F.G. Joachim (1975) Photoperiodic induction of the pupal diapause in the tobacco hornworm, Manduca sexta. J. Insect Physiol. 21: 1471-1480.

Bonnemaison, L. (1975) Action de la photopériode sur l'induction de la diapause chez Mamestra brassicae (Lép. Noctuidae. Ann. Soc. Entomol. Fr. (N.S.) 11: 767-781.

Bradshaw, W.E. (1974) Photoperiodic control of development in Chaoborus americanus with special reference to photoperiodic action spectra. Biol. Bull. 146: 11-19.

Bradshaw, W.E. , and C.M. Holzapfel (1977) Interaction between photoperiod, temperature and chilling in dormant larvae of the tree-hole mosquito, Toxorhynchites rutilus Coq. Biol. Bull. 152: 147-158.

Bradshaw, W.E. , and L.P. Lounibos (1972) Photoperiodic control of development in the pitcher-plant mosquito, Wyeomyia smithii. Can. J. Zool. 50: 713-719.

10.

Brunnarius, J. , and B. Dumortier (1984) Existence of a light-sensitive phase in the photoperiodic termination of diapause in Pieris brassicae L. (Insecta: Lepidoptera) and comparison with diapause induction. J. Comp. Physiol. A 155: 161-169.

11.

Claret, J. (1985) Two mechanisms in the biological clock of Pieris brassicae L.: An oscillator for diapause induction; an hour-glass for diapause termination. Experientia 41: 1613-1615.

12.

Duelli, P. (1986) Diapause induction in Chrysoperla carnea: What photoperiodical parameters are actually measured? In Ecology of Aphidophaga, I. Hodek , ed., pp. 239-244, Academia, Prague, and W. Junk , Dordrecht.

13.

Dumortier, B. , and J. Brunnarius (1981) Involvement of the circadian system in photoperiodism and thermoperiodism in Pieris brassicae (Lepidoptera. In Biological Clocks in Seasonal Reproductive Cycles, B. K. Follett and D. E. Follett , eds., pp. 83-99, Wright, Bristol.

14.

Dumortier, B. , and J. Brunnarius (1987) Photoperiodic time measurement in an insect: Is the photoinducible phase a reality? In Comparative Physiology of Environmental Adaptations, Vol. 3, P. Pévet , ed., pp. 1-22, S. Karger, Basel.

15.

Evans, K.W. , and R.A. Brust (1972) Induction and termination of diapause in Wyeomyia smithii (Diptera: Culicidae), and larval survival studies at low and sub-zero temperatures. Can. Entomol. 104: 1937-1950.

16.

Furunishi, S. , S. Masaki , Y. Hashimoto , and M. S-Zuki (1982) Diapause responses to photoperiod and night interruption in Mamestra brassicae. Appl. Entomol. Zool. 17: 398-409.

17.

Gnagey, A.L. , and D.L. Denlinger (1984) Photoperiodic induction of pupal diapause in the flesh fly, Sarcophaga crassipalpis: Embryonic sensitivity. J. Comp. Physiol. B 154: 91-96.

18.

Gotoh, T. (1986) Termination pattern of diapause in the two-spotted spider mite, Tetranychus urticae Koch (Acarina: Tetranychidae) in Sapporo . Appl. Entomol. Zool. 21: 480-481.

19.

Hayes, D.K. , B.M. Cawley , W.N. Sullivan , V.E. Adler , and M.S. Schechter (1974) The effect of added light pulses on overwintering and diapause, under natural light and temperature conditions, of four species of Lepidoptera. Environ. Entomol. 3: 863-865.

20.

Hayes, D.K. , W.N. Sullivan , B.M. Cawley , M.Z. Oliver , and M.S. Schechter (1970) Delay and acceleration of breaking diapause of Antheraea pernyi and Laspeyresia pomonella by photoperiod manipulation. Life Sci. 9: 601-606.

21.

Hidaka, T. , and Y. Hirai (1970) Effect of non-24-hour photoperiod and light interruption of the dark phase on diapause determination in Papilio xuthus L. Proc. Japan Acad. 46: 541-545.

22.

Hodek, I. (1983) Role of environmental factors and endogenous mechanisms in the seasonality of reproduction in insects diapausing as adults. In Diapause and Life Cycle Strategies in Insects, V. K. Brown and I. Hodek , eds., pp. 9-33, W. Junk, The Hague .

23.

Kono, Y. (1970) Photoperiodic induction of diapause in Pieris rapae crucivora Boisduval (Lepidoptera; Pieridae. Appl. Entomol. Zool. 5: 213-224.

24.

Koveos, D.S. , A. Kroon , and A. Veerman (1993) Geographic variation of diapause intensity in the spider mite Tetranychus urticae. Physiol. Entomol. 18: 50-56.

25.

Lavialle, M. (1988) La symétrie des réponses photopériodiques dans l'induction et la terminaison de diapause chez Ostrinia nubilalis Hbn. (Lep., Pyralidae. J. Appl. Entomol. 105: 516-524.

26.

Lees, A.D. (1966) Photoperiodic timing mechanisms m insects. Nature 210: 986-989.

27.

Masaki, S. (1984) Unity and diversity in insect photopenodism. In Photoperiodic Regulation of Insect and Molluscan Hormones, R. Porter and G. M. Collins , eds., Ciba Foundation Symposium No. 104, pp. 7-25, Pitman, London.

28.

Masaki, S. , and S. Kikukawa (1981) The diapause clock in a moth: Response to temperature signals. In Biological Clocks in Seasonal Reproductive Cycles , B. K. Follett and D. E. Follett , eds., pp. 101-112, Wright, Bristol.

29.

Masaki, S. , and Y. Watari (1989) Response to night interruption in photoperiodic determination of wing form of the ground cricket Dianemobius fascipes. Physiol. Entomol. 14: 179-186.

30.

Numata, H. , and T. Hidaka (1982) Photoperiodic control of adult diapause in the bean bug, Riptortus clavatus Thunberg (Heteroptera: Coreidae): I. Reversible induction and termination of diapause. Appl. Entomol. Zool. 17: 530-538.

31.

Numata, H. , and T. Hidaka (1984) Photoperiodic control of adult diapause in the bean bug Riptortus clavatus Thunberg (Heteroptera: Coreidae): III. Diapause development and temperature. Appl. Entomol. Zool. 19: 356- 360.

32.

Numata, H. , and T. Hidaka (1987) Photoreceptors for photoperiodism in the bean bug , Riptortus clavatus. Rostria 38: 571-580.

33.

Saunders, D.S. (1968) Photoperiodism and time measurement in the parasitic wasp, Nasonia vitripennis. J. Insect Physiol. 14: 433-450.

34.

Saunders, D.S. (1982) Insect Clocks, 2nd ed., Pergamon Press, Oxford.

35.

Saunders, D.S. (1983) A diapause induction-termination asymmetry in the photoperiodic response of the linden bug Pyrrhocoris apterus and an effect of near critical photoperiods on development. J. Insect Physiol. 29: 399-405.

36.

Saunders, D.S. (1987) Insect photoperiodism: The linden bug, Pyrrhocoris apterus, a species that measures daylength rather than nightlength. Experientia 43: 935-937.

37.

Skopik, S.D. , and M. Takeda (1986) Photoperiodic control of diapause induction and termination in Ostrinia nubilalis: Two different clocks? J. Biol. Rhythms 1: 137-143.

38.

Skopik, S.D. , M. Takeda , W.J. Cain , and N.G. Patel (1986) Insect photoperiodism: Diversity of results in night-break experiments, including nonresponsiveness to light. J. Biol. Rhythms 1: 243-249.

39.

Smith, S.M. , and R.A. Brust (1971) Photoperiodic control of the maintenance and termination of larval diapause in Wyeomyia smithii (Coq.) (Diptera: Culicidae) with notes on oogenesis in the adult female. Can. J. Zool. 49: 1065-1073.

40.

Takeda, M. (1985) An "hourglass-like" feature in the photoperiodic time measurement in Diatraea grandiosella (Pyralidae. J. Insect Physiol. 31: 397-406.

41.

Tauber, M.J. , C.A. Tauber , and S. Masaki (1986) Seasonal Adaptations of Insects, Oxford University Press, New York.

42.

Teetes, G.L. , P.L. Adkisson , and N.M. Randolph (1969) Photoperiod and temperature as factors controlling the diapause of the sunflower moth, Homoeosoma electellum. J. Insect Physiol. 15: 755-761.

43.

Van Houten, Y.M. , and R.L. Veenendaal (1990) Effects of photoperiod, temperature, food and relative humidity on the induction of diapause in the predatory mite Amblyseius potentillae. Exp. Appl. Acarol. 10: 111-128.

44.

Vaz Nunes, M. , and J. Hardie (1987) An instantly damping oscillator model for photoperiodic time measurement in the aphid Aphis fabae. J. Insect Physiol. 33: 831-841.

45.

Vaz Nunes, M. , D.S. Koveos , and A. Veerman (1990) Geographical variation in the photoperiodic induction of diapause in the spider mite (Tetranychus urticae): A causal relation between critical nightlength and circadian period? J. Biol. Rhythms 5: 47-57.

46.

Vaz Nunes, M. , and A. Veerman (1979) Photoperiodic time measurement in spider mites: II. Effects of skeleton photoperiods. J. Comp. Physiol. 134: 219-226.

47.

Vaz Nunes, M. , and A. Veerman (1982) Photoperiodic time measurement in the spider mite Tetranychus urticae: A novel concept. J. Insect Physiol. 28: 1041-1053.

48.

Vaz Nunes, M. , and A. Veerman (1984) Light-break experiments and photoperiodic time measurement in the spider mite Tetranychus urticae. J. Insect Physiol. 30: 891-897.

49.

Vaz Nunes, M. , and A. Veerman (1986a) A "dusk" oscillator affects photoperiodic induction of diapause in the spider mite Tetranychus urticae. J. Insect Physiol. 32: 605-614.

50.

Vaz Nunes, M. , and A. Veerman (1986b) Similarities between the photoperiodic clocks of Megoura and Tetranychus: Experiments with spider mites. J. Insect Physiol. 32: 1029-1034.

51.

Vaz Nunes, M. , and A. Veerman (1987) Photoperiodic time measurement in a Russian strain of the spider mite Tetranychus urticae. J. Insect Physiol. 33: 533-541.

52.

Veerman, A. (1977a) Aspects of the induction of diapause in a laboratory strain of the mite, Tetranychus urticae. J. Insect Physiol. 23: 703-711.

53.

Veerman, A. (1977b) Photoperiodic termination of diapause in spider mites. Nature 266: 526-527.

54.

Veerman, A. (1985) Diapause. In Spider Mites: Their Biology, Natural Enemies and Control, Vol. lA, W. Helle and M. W. Sabelis , eds., pp. 279-316, Elsevier, Amsterdam.

55.

Veerman, A. (1991) Physiological aspects of diapause in plant-inhabiting mites. In The Acari: Reproduction, Development and Life-History Strategies, R. Schuster and P. W. Murphy , eds., pp. 245-265, Chapman & Hall, London.

56.

Veerman, A. , and D.S. Koveos (1989) Separation of photoperiodic and circadian effects on the termination of diapause in the spider mite Tetranychus urticae. Experientia 45: 1143-1146.

57.

Veerman, A. , and M. Vaz Nunes (1987) Analysis of the operation of the photoperiodic counter provides evidence for hourglass time measurement in the spider mite Tetranychus urticae. J. Comp. Physiol. A 160: 421-430.

58.

Williams, C.M. , and P.L. Adkisson (1964) Physiology of insect diapause: XIV. An endocrine mechanism for the photoperiodic control of pupal diapause in the oak silkworm Antheraea pernyi. Biol. Bull. 127: 511-525.

59.

Zaslavski, V.A. (1988) Insect Development: Photoperiodic and Temperature Control, Springer-Verlag, New York .