M. Vaz Nunes

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.

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.

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”.

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.

A coupled oscillator feedback system as a model for the photoperiodic clock in insects and mites. II. Simulations of photoperiodic responses

A model is described for the photoperiodic clock in insects and mites based on a circadian “pacemaker-slave” system, in which both the pacemaker and the slave are entrainable by light and by temperature. The pacemaker is self-sustained or slightly damped, whereas the slave is heavily damped and coupled to the pacemaker. It is proposed that the actual nightlength measurement is performed by the slave. Under certain circumstances the pacemaker may disturb the accumulation of photoperiodic information contained in subsequent light-dark cycles. Model-generated response curves parallel those found in a diversity of photoperiodic experiments performed with insects and mites as known from the literature.

A coupled oscillator feedback system as a model for the photoperiodic clock in insects and mites. I: The basic control system as a model for circadian rhythms

A control systems model for the photoperiodic clock is developed, which is an extended version of the earlier published “damped circadian oscillator model”, and which consists of two feedback circadian oscillators, a “pacemaker” and a “slave”, both entrainable by light and by temperature. The pacemaker is self-sustained or slightly damping, and the slave, which is coupled to the pacemaker, is strongly damped. The coupling is such, that with stronger coupling the slaves amplitude increases and the oscillation becomes less damped. In the first paper we demonstrate that the model is capable of describing many features of circadian rhythms, such as the occurrence of transients in constant darkness after a single light pulse, temperature-compensated shapes of phase response curves of both type 1 (weak resetting) and type 0 (strong resetting), and changes in pacemaker-slave phase relations when entrained by light-dark cycles with increasing photophases.

Light-break experiments and photoperiodic time measurement in the spider mite Tetranychus urticae

Abstract To explain photoperiodic induction of diapause in the spider mite Tetranychus urticae (Acarina: Tetranychidae) a theoretical model was developed, consisting of two components, viz. a “clock” and a photoperiodic “counter” mechanism. The clock executes photoperiodic time measurement according to hourglass kinetics; the counter accumulates the photoperiodic information contained in a number of successive light dark cycles by adding up the number of “long” and “short” nights experienced by the developmental stages of the mites sensitive to the photoperiod. The influence of the circadian system on photoperiodic induction is interpreted as an inhibitory effect exerted on the expression of the photoperiodic response; this effect is encountered only in certain photoperiodic regimes, where the circadian system and the photoperiod are out of “resonance” with each other. This “hourglass timer oscillator counter model”, devised to give a theoretical explanation of photoperiodic time measurement, the summation of photoperiodic information, and the influence of the circadian system on photoperiodic induction, proved to be consistent with experimental results obtained with T. urticae in both symmetrical and asymmetrical “skeleton” photoperiods, the latter based on diel as well as non-diel light dark cycles.

Similarities between the photoperiodic clocks of Megoura and Tetranychus: Experiments with spider mites

Abstract According to the “hourglass timer-oscillator counter” model, photoperiodic time measurement in the spider mite Tetranychus urticae is performed by a non-oscillatory or hourglass clock. The main characteristics of the spider mites clock are the same as those of the hourglass timer developed by Lees (1973) for the aphid, Megoura viciae; the hourglass clock, applied in the spider mites model, may be regarded as a redescription in mathematical terms of Leess word model. To investigate the similarity between the photoperiodic clocks of Tetranychus and Megoura, some experiments which had been specifically designed by Lees to test the hourglass concept in Megoura have been repeated with Tetranychus. Experimental results were compared, both with the results of similar experiments with M. viciae, and with predictions based on the “hourglass timer-oscillator counter” model. A close resemblance was found between the results obtained with both species, which shows that photoperiodic time measurement in the spider mite and the aphid is accomplished by photoperiodic clocks the kinetics of which have much in common and may, apart from velocity parameters, even be principally the same. In the instances where differences were observed, these appeared to be attributable for the most part (according to the “hourglass timer-oscillator counter” model) to the influence of the circadian system which, in certain regimes, may strongly affect photoperiodic induction in T. urticae, but which has no detectable influence in M. viciae.

Photoperiodic time measurement in spider mites

SummaryA model has been developed which describes in mathematical terms the incidence of diapause in the spider miteTetranychus urticae under different photoperiodic regimens. The model has been derived from Becks (1974a, b, 1975, 1976a) ‘Dual System Theory’ of photoperiodic time measurement, by means of a number of essential alterations and modifications. The spider mites model is composed of two ‘hour-glass’ timers, one of which starts at lights-off and ‘measures’ the length of the night, whereas the other is initiated both by the onset of the first hour-glass timer and by lights-on. This second hour-glass defines the time at which the first hour-glass is ‘read off’, the state of the first hour-glass at this particular time being decisive for the developmental alternative (diapause or nondiapause) to be determined. The model may be classified as a form of ‘internal coincidence’ according to the terminology of Pittendrigh (1972), since it is based on the interaction of two internal systems rather than on the coincidence of light with a particular light-sensitive phase of the timing mechanism, as in the case of ‘external coincidence’ (cf. Saunders, 1978). Good agreement is attained between diapause incidences predicted by this model and incidences observed in spider mites, both in the diapause induction response curve and in asymmetrical skeleton photoperiods.

External coincidence and photoperiodic time measurement in the spider mite Tetranychus urticae

Abstract The incidence of diapause in the spider mite Tetranychus urticae was predicted for various photoperiodic regimes, according to the external coincidence model of photoperiodic time measurement. A phase response curve was constructed for the hypothetical photoperiodic oscillator in these mites: entrainment of this photoperiodic oscillator to a variety of ‘complete’ and ‘skeleton’ photoperiods was calculated using a transformation method for circadian rhythms. The external coincidence model proved adequate to describe experimental results with T. urticae in ‘complete’ photoperiods ( T = 24 hr), symmetrical ‘skeleton’ photoperiods ( T = 24 hr), asymmetrical ‘skeleton’ photoperiods ( T = 24 hr) (night-interruption experiments), and ‘resonance’ experiments, in which the light component of a light/dark cycle was held constant at 8 hr and the dark component was varied over a wide range in successive experiments, providing cycles with period lengths up to 92 hr. The external coincidence model proved inadequate to explain results obtained in a ‘ T -experiment’ with T. urticae comprising 1 hr pulses of light in a cycle of L D 1 :17.5 ( T = 18.5 hr) with the first pulse of the train starting at different circadian phases. The validity and limitations of the external coincidence model as an explanation of photoperiodic time measurement in T. urticae are discussed in view of the above results.