A. Veerman

Photoperiodic time measurement in the spider mite Tetranychus urticae: A novel concept

Abstract To explain photoperiodic induction of diapause in the spider mite Tetranychus urticae a new theoretical model was developed which took into account both the hourglass and rhythmic elements shown to be present in the photoperiodic reaction of these mites. It is emphasized that photoperiodic induction is the result of time measurement as well as the summation and integration of a number of successive photoperiodic cycles: the model, therefore, consists of separate ‘clock’ and ‘counter’ mechanisms. In current views involvement of the circadian system in photoperiodism is interpreted in terms of the hypothesis that the photoperiodic clock itself is based on one or more circadian oscillators. Here a different approach has been chosen as regards the role of the circadian system in photoperiodism: the possibility, previously put forward by other authors, that some aspect of the photoperiodic induction mechanism other than the clock is controlled by the circadian system was investigated by assuming a circadian influence on the photoperiodic counter mechanism. The derivation of this ‘hourglass timer oscillator counter’ model of photoperiodic induction in T. urticae is described and its operation demonstrated on the basis of a number of diel and nondiel photoperiods, with and without light interruptions.

Aspects of the induction of diapause in a laboratory strain of the mite Tetranychus urticae

Some diapause characteristics were studied in a strain of the spider mite. Tetranychus urticae. which had been reared on bean plants in the laboratory for over 15 yr. The diapause induction response curve was of the long-day type, showing a sharply defined critical daylength of 13 hr 50 min. In constant darkness no diapause induction occurred, but with a photoperiod of 1L:23D diapause incidence was already complete. A thermoperiod with a 5°C amplitude induced diapause in combination with a short-day photoperiod only when the low phase of the thermoperiod coincided with the scotophase. The same thermoperiod did not induce any diapause in constant darkness. The photoperiodic reaction of the laboratory strain used in these experiments appeared to remain constant over a very long period of time and to be independent of the diapause history of previous generations of mites. Although photoperiodic sensitivity was demonstrated during the whole postembryonic development, sensitivity was maximal at the end of the protonymphal instar and declined rapidly during the deutonymphal instar. Only 2 inductive cycles of 10L:14D were required to induce up to 62% diapause if the mites were kept in continuous darkness during the remainder of their development. Long days or continuous light could reverse the inductive effect of a sequence of short-day cycles previously applied to the mites. Light breaks of 1 hr duration applied at different times during the dark period of a 10L:14D photoperiod generated a sharp bimodal response curve with two discrete points of sensitivity to the light breaks at 10 hr after ‘dusk’ and 10 hr before ‘dawn’, thus showing a remarkable similarity with the results obtained in light break experiments with some species of insects.

Analysis of the operation of the photoperiodic counter provides evidence for hourglass time measurement in the spider miteTetranychus urticae

SummaryPhotoperiodic induction of diapause in the spider miteTetranychus urticae is the net result of at least two processes: time measurement (the photoperiodic ‘clock’) and the accumulation of the photoperiodic information contained in a sequence of light-dark cycles (the photoperiodic ‘counter’). In this paper an analysis is presented of the operation of the photoperiodic counter in the spider mite.1.Mites which experienced a sequence of longnight cycles during their entire sensitive period showed 100% diapause; no diapause was observed in continuous darkness. When an increasing number of long-night cycles was applied to the mites against a ‘background’ of continuous darkness, diapause incidence was found to rise steadily: only 3 cycles sufficed to induce diapause in about half the population, whereas a minimal number of 6 cycles was required for 90–100% diapause to be attained. At the test temperature of 18.5°C the sensitive period lasted 11–12 days, comprising the complete post-embryonic developmental period, up to the final moult. Photoperiodic sensitivity was found to vary slightly over the whole sensitive period of the mites, the highest sensitivity being observed around days 3–6.2.Short-night cycles were also shown to be accumulated, but with an effect opposite to that of long-night cycles. If the mites received a number of short-night cycles before being transferred to a long-night regime, the effect of the short-night cycles had to be levelled first by a number of longnight cycles, before the accumulation of the diapause-inducing effect of the long-night cycles was started.3.Special attention has been given to the effect of the aperiodic signals continuous light and continuous darkness. It could be shown that continuous light has a slightly reversing effect on diapause induction if applied after a series of long-night cycles; continuous light is more or less ‘neutral’ (i.e. neither reversing nor promoting diapause induction) if it precedes the long-night cycles.4.In experiments in which the effects of continuous light and continuous darkness were compared it could be shown that continuous darkness is equivalent to one long night: the minimal number of long-night cycles required for diapause induction was found to be one more if the long-night cycles were given after the mites had received continuous light instead of continuous darkness during the first part of the sensitive period.5.A critical test, based on the photoperiodic counter principle and devised to discriminate between single and repeated nightlength measurements (using nights of 12 h and 36 h long), showed that all nights are counted only once, irrespective of their lengths: all nights longer than the critical nightlength were found to be about equally inductive. This shows that the photoperiodic clock in the spider mite does not operate according to oscillator kinetics: a clock of the oscillator type resets itself in longer dark phases and would have performed two consecutive acts of time measurement in a night of 36 h long. Consequently, the photoperiodic clock inT. urticae is either an hourglass or an instantly damped circadian oscillator, the kinetics of either of which would produce the results observed in the experiments reported here.

Functional involvement of carotenoids in photoperiodic induction of diapause in the spider mite, Tetranychus urticae.

ABSTRACT. Using pigment mutants in which the uptake and oxidative metabolism of β‐carotene is disturbed, it could be shown that carotenoid pigments are functionally involved in the photoperiodic reaction in the spider mite, Tetranychus urticae Koch (Acari; Prostigmata). Diapause responses appeared to be lowered in four albino mutants in comparison with the wild‐type strains from which they originated. Back‐crossing of the albino mutants to wild‐type for ten generations did not restore the capability to diapause. Selection for diapause for six generations also proved unsuccessful in increasing the diapause response of the albino strains. On the other hand, albino mites coming from hybrid (phenotypically wild‐type) mothers all diapaused normally. Apparently a maternal effect is responsible for the complete induction of diapause in albino mites. It is supposed that minimal amounts of carotenoids of maternal origin suffice in the embryo for the formation of a photopigment concerned in the photoperiodic induction of diapause. In albino mites the normal transmission of carotenoids via the egg is probably blocked. This transmission of pigment seems to be restored when the albinos originate from hybrid mothers, which possess the wild pigmentation.

A “dusk” oscillator affects photoperiodic induction of diapause in the spider mit, Tetranychus urticae

Abstract Both a “clock” role and a “non-clock” role have been suggested for the circadian component in seasonal photoperiodism. The non-clock hypothesis is based on the idea that the circadian system may affect the expression of a photoperiodic response, without being involved in photoperiodic time measurement itself. When the circadian system and the environmental light-dark cycle are “out of resonance”, internal temporal order is thought to be disrupted, which may have a deleterious effect on the photoperiodic mechanism. An explicit model, based on the above “resonance” hypothesis, is the “hourglass timer-oscillator counter model”, developed to explain photoperiodic induction of diapause in the spider mite Tetranychus urticae . In previous papers the model was shown to give an excellent description of a variety of photoperiodic experiments performed with spider mites. In this paper the validity of the model is tested for a large series of so-called resonance experiments. In these experiments the length of the light period is held constant and the dark component is varied over a wide range to provide light-dark cycles of up to 72 h or more in length. The response curves obtained with constant photophases of 1, 2, 4, 8, 12, 16, 20 and 24 h revealed four to five maxima and minima of diapause incidence, with peak to peak intervals of about 20 h. The results were redrawn in the form of an “extended circadian topography”, from which it was concluded that the observed rhythmicity is caused by a “dusk” oscillator. In two resonance experiments with constant scotophases of, respectively, 10 and 12 h, combined with photophases varying in length from 1 to 60 h, no sign of rhythmicity was found in the resulting response curves. For all experiments a close agreement was found between experimental results and predictions based on the “hourglass timer-oscillator counter model”.

Selection for non-diapause in Amblyseius cucumeris and Amblyseius barkeri and exploration of the effectiveness of selected strains for thrips control

In Europe and North America the western flower thrips, Frankliniella occidentalis, is an important pest in various greenhouse crops, such as sweet pepper and cucumber. Two species of predatory mite are commercially applied for biological control of this pest: Amblyseius cucumeris and A. barkeri. Thrips control is generally successful from March onwards. During winter, however, thrips control by these predatory mites is less effective. An important reason for this is that the commercially applied strains of both mite species enter reproductive diapause under short‐day photoperiods, whereas the western flower thrips does not enter diapause. In this paper we report on selection experiments for non‐diapause in strains of both mite species, aimed at obtaining predators that do not enter diapause under light‐ and temperature conditions prevailing in winter. Additional experiments were done to estimate the potential of the selected lines as control agents of F. occidentalis. Selection for non‐diapause proved highly successful in both predatory mite species. In a New Zealand strain of A. cucumeris diapause incidence decreased from 41% to 0% in about ten generations; in a Dutch strain of A. barkeri diapause incidence decreased from 67% to 0% in about six generations. Furthermore, selection for non‐diapause had no influence on predator performance, measured as predation rate and oviposition rate on a diet of first instar thirps larvae. Rates of predation and oviposition were the same for selected and unselected lines in both species; rates of predation and oviposition were higher for A. cucumeris than for A. barkeri. After 18 months under non‐diapause conditions, no less than 92% of a sample of the selected non‐diapause line of A. cucumeris did not enter diapause when tested under diapause‐inducing conditions. This indicates that ‘non‐diapause’ is a stable trait in these predatory mites. Finally, a small‐scale greenhouse experiment in a sweet pepper crop showed that the selected non‐diapause line of A. cucumeris established successfully under diapause‐inducing short‐day conditions.

Thermoperiodic induction of diapause in the predacious mite, Amblyseius potentillae

Abstract The effect of temperature on the induction of diapause was studied in the phytoseiid mite Amblyseius potentillae . Photoperiodic induction of diapause was shown to be temperature dependent; at higher constant temperatures diapause incidence was virtually absent. When a photoperiod was applied in combination with a thermoperiod, diapause was induced only if the cool phase of the thermoperiod coincided with the scotophase; scotophase temperature appeared to be of much greater importance for diapause induction than photophase temperature. For the first time in a mite it was shown that diapause could be induced by a thermoperiod in continuous darkness. No diapause or only a very low incidence of diapause was found in continuous darkness when either the high, mean or low temperature of the thermoperiod was applied as a constant temperature throughout. A thermoperiodic response was found to be absent in continuous light. The thermoperiodic response curve determined for A. potentillae appeared to be closely similar to the photoperiodic response curve. Both the critical scoto- and cryophase were about 10 h in duration. Incidence of diapause was found to be dependent on the amplitude of the thermoperiod; except for the higher temperature range diapause incidence increased with increasing thermoperiod amplitude. Full induction of diapause was obtained with an amplitude of 4°C and above. No indication was found for the existence of a temperature threshold for thermoperiodic induction of diapause in A. potentillae .

Geographical variation in photoperiodic induction of diapause in the spider mite (Tetranychus urticae): a causal relation between critical nightlength and circadian period?

The photoperiodic response of 10 strains of the two-spotted spider mite (Tetranychus urticae), originating between 40.5° and 60°N in Western and Central Europe, was found to be highly variable. The critical nightlength for photoperiodic induction of diapause was strongly correlated with latitude for the lowland populations and varied from 7.75 hr in the north to 13.25 hr in the south. The length of the circadian period, taken as the peak-to-peak interval in response curves of resonance experiments done with T. urticae, varied between 17.75 and 21.5 hr and appeared weakly correlated with latitude. Only a very weak correlation was observed between critical nightlength and circadian period. These results do not provide evidence in favor of a circadian-based photoperiodic clock in T. urticae. On the other hand, they also do not refute this possibility, as there may be other circadian or noncircadian factors affecting the critical nightlength, which could mask the influence of circadian period.

Geographic variation of diapause intensity in the spider mite Tetranychus urticae

Abstract. Eight strains of the spider mite Tetranychus urticae, originating from different localities in western and central Europe, with latitudes ranging from 40.5 to 60oN, displayed marked differences in the period of chilling at 4oC required for diapause termination under a diapause‐maintaining short‐day photoperiodic regime at 19oC, to which the mites were transferred after the cold period. The higher the latitude from which the strains originated the longer was the period of chilling required for diapause termination, suggesting the presence of a gradient in diapause intensity, diapause being deeper the more northern the origin of the strains.

Photoperiodic induction of diapause in the large white butterfly, Pieris brassicae: Evidence for hourglass time measurement

Abstract Diapause incidence in pupae of the large white butterfly, Pieris brassicae , showed an increase from 0 to 100% when the larvae experienced an increasing number of long-night cycles during their sensitive period, while being kept in continuous darkness during the remainder of their development. About 5 long nights sufficed to induce diapause in 50% of the insects; 7 long-night cycles were required to raise diapause incidence to 100%. When the summation of cycles with nightlengths of 16 and 40 h was compared, the inductive “strength” of nights of 16 and 40 h long appeared to be about the same. This means that nights of 40 h long are not measured twice by the photoperiodic clock, which would have been expected if the clock were a circadian oscillator or a complex of circadian oscillators. These experiments show that the photoperiodic clock in P. brassicae is not a self-sustained oscillator, but more likely an hourglass. In resonance experiments with a constant photophase of 8 h and a variable dark phase a circadian influence on photoperiodic induction was found at 22.5°C, but not at 19°C. Measurement of the critical nightlength was equally sharp in resonance experiments at both temperatures, however. The above results are best explained by the “hourglass timer-oscillator counter model” or “resonance model” for photoperiodic induction of diapause, originally developed for the spider mite Tetranychus urticae .