Existence of a light-sensitive phase in the photoperiodic termination of diapause inPieris brassicae L. (Insecta:Lepidoptera) and comparison with diapause induction

Summary Pupal diapause ofPieris brassicae can be terminated experimentally by the sole action of photoperiod. Curves gave evidence of similar effect of photoperiod within a broad range of regimes in both diapause induction and termination. However, they showed opposite responses to ultra-short and ultra-long days and to continuous light and darkness. In diapause termination, the critical daylength is longer than in diapause induction by about 1.20 h.Results of night interruption experiments (asymmetrical skeleton photoperiods) provided the first reliable evidence of the involvement of a particular light-sensitive phase in photoperiodic diapause termination. A light pulse delivered at this moment elicited a complete long-day effect (i.e. diapause termination). Only one single point of long-day effect (lying in the early night) was disclosed in diapause termination whereas two points (A and B) characterize diapause induction in this species. Results of experimental designs where the period of the photoperiodic cycles differed from 24 h indicated that photoperiodic clock likely makes a nightlength measurement in both diapause induction and termination. This is discussed in relation to the formal properties of the clock, especially those derived from the time distribution of points of long-day effect.     

In vivo and in vitro photoperiodic induction of diapause using isolated brain-suboesophageal ganglion complexes of the silkworm,Bombyx mori

By use of a bivoltine silkworm race which shows a long-day photoperiodic response after induction during the last (5th) instar, we tried to programme photoperiodic induction in the isolated brain-suboesophageal ganglion complex in vivo and in vitro. A pair of the complexes from a newly ecdysed 5th-instar female was transplanted into the abdomen of a late 5th-instar larva and exposed to long-day (20 h light: 4 h dark) or short-day (8 h light: 16 h dark) conditions for 3 cycles. The short-day-exposed complexes elicited the production of diapause eggs in the recipient silkworms destined to become non-diapause egg producers, whereas the long-day-exposed brain complexes produced non-diapause eggs. Transplant experiments of the brain-suboesophageal ganglion complex using isolated abdomens showed a similar result. The brain complexes from newly ecdysed females of the 5th-instar were cultured in Grace's insect medium under 20 h light: 4 h dark or 8 h light: 16 h dark for 4 cycles, respectively. After in vitro culture, a pair of complexes was implanted into the abdomen of a late 5th-instar larva destined to become a non-diapause egg producer, and the diapause incidence in the resultant moths was examined. The brain complexes which received the short-day cycles induced a large portion of diapause eggs, whereas those which received the long-day conditions induced non-diapause eggs. The connection of corpora cardiaca and corpora allata with the brain complex had no influence on the result. Suboesophageal ganglia which had been cultured in vitro and implanted elicited a remarkable production of diapause eggs, but cultured brains were ineffective in producing diapause eggs, regardless of the photoperiod experienced. These results demonstrate that photoperiodic induction of the silkworm can be programmed in in vivo and in vitro culture systems, and that components of the photoperiodic clock (photoreceptor, clock, and counter system) are located in the brain-suboesophageal ganglion complex, possibly in the brain itself.     

Photoperiodic Control of Developmental Diapause in Nymphs of Prostriate Ixodid Ticks (Acari: Ixodidae)

Extrinsic control of developmental diapause in nymphs of prostriate ticks of the subgenus Ixodes sensu stricto (Ixodes ricinus and Ixodes persulcatus from Eurasia and Ixodes scapularis from North America) appears to be based on a complex two-step photoperiodic reaction of a short-day/long-day type. Diapause control in the subgenus Afrixodes (the South African tick Ixodes rubicundus) appears to be based on a simple long-day reaction. The option between non-diapause development and diapausing arrest in engorged nymphs is determined by both pre- and post-feeding photoperiodic regimes. Consequently diapausing arrest in engorged nymphs of Ixodes sensu stricto can be induced either by a short-day (after their engorgement) or by a long-day regime (in unfed nymphs), while active, non-diapause development is possible only when the short-day pre-feeding regime is followed by a long-day post-feeding regime. The photoperiodic response in I. (Afrixodes) rubicundus nymphs seems to be of the long-day type both before and after feeding. Consequently this non-diapause development is enabled by a long-day regime, while diapause is induced by a short-day regime of exposure. Nevertheless, there are some indications that the control of nymphal diapause in the latter species is also of a complex nature. This revised version was published online in July 2006 with corrections to the Cover Date.     

Induction and termination of diapause inOrius predatory bugs

Photoperiodic induction of reproductive diapause at 18°C was investigated in fourOrius [Heteroptera: Anthocoridae] species.Orius insidiosus (Say) displayed a long-day response with a critical photoperiod between L11:D13 and L12:D12. Diapause in this species was terminated rapidly when the temperature and/or the daylength were increased.Orius majusculus (Reuter) also displayed a long-day response. The critical photoperiod fell between L14:D10 and L16:D8. Diapause in this species was not terminated within 14 days when both temperature and daylength were increased. InOrius albidipennis (Reuter) no diapause could be induced at photoperiods varying from L8:D16 to L16:D8. InOrius tristicolor (White) a high proportion of diapause was found at all photoperiods tested. The effect of temperature on photoperiodic induction of diapause was studied inO. insidiosus at L10:D14. Diapause occurred at 18°C, 21°C and 25°C, but not at 30°C. Again, diapause was terminated rapidly after transfer to 25°C/L16:D8. Exposing only the nymphal instars 1–5 to short daylength was not enough to induce diapause in the whole population ofO. majusculus. Orius predatory bugs are used as biocontrol agents against western flower thrips,Frankliniella occidentalis (Pergande) [Thysanoptera: Thripidael, in greenhouses. The consequences of photoperiodic induction of diapause for the success of early season releases ofOrius are discussed.     

Localization of the photoreceptor for photoperiodism in the stink bug, Plautia crossota stali

The brown-winged green bug Plautia crossota stali Scott (Heteroptera: Pentatomidae) shows a long-day photoperiodic response with respect to the control of adult diapause. The location of the photoreceptor for this response was examined by surgical removal of putative photoreceptor organs. Even after both ocelli were removed, the insects responded normally to the photoperiod. After bilateral removal of the compound eyes, the insects developed reproductive organs and the volume of the corpus allatum increased regardless of photoperiod. Therefore, the compound eyes play a major role in the reception of photic information for photoperiodism in P. c. stali. However, because removal of the bilateral compound eyes did not completely prevent the response to photoperiod, photoreceptors other than the compound eyes can also receive photic information for photoperiodism.     

Some aspects of induction and termination of diapause in a Greek strain of the miteTetranychus cinnabarinus (Boisduval) Boudreaux, 1956 (Acari: Tetranychidae)

A Greek strain of the miteTetranychus cinnabarinus, collected from ivy (Hedera spec.) in Thessaloniki (41 °N), exhibits a facultative, imaginal diapause. Diapause is induced by photoperiod and the photoperiodic response is of the long-day type. The critical daylength is 12.5 h at 19 °C. A period of chilling is not necessary for the termination of diapause under long-day conditions. Diapausing females are sensitive to photoperiod at least during the first 11/2 month of diapause.     

Induction of reproductive diapause via perception of photoperiod through the compound eyes in the adult blow fly, Protophormia terraenovae

Covering and surgical removal of the compound eyes were performed to localize photoreceptors for photoperiodic responses in the blow fly Protophormia terraenovae (Diptera, Calliphoridae). Adult females showed a long-day photoperiodic response to control reproductive diapause. When the compound eyes were bilaterally covered with silver paint, diapause incidence increased under diapause-preventing conditions, i.e., a long-day photoperiod and constant light, as though flies were kept under constant darkness. Neither silver painting on a medial region of the head capsule nor control painting in which both compound eyes were painted in a clear solvent caused significant effects on diapause incidence. Unilateral painting of the compound eye caused an increment of diapause incidence under constant light but no effects under a long-day photoperiod. When the compound eyes were bilaterally removed, all the flies developed their ovaries both under a long-day and a short-day photoperiod. Unilateral removal of the compound eye also caused ovarian development under a short-day photoperiod, whereas removal of one antennal lobe or all ocelli caused no effects on diapause incidence. Since P. terraenovae completely lost responsiveness to photoperiod after blinding of the compound eyes, it is likely that this fly perceives photoperiod through its compound eyes. Accepted: 18 February 1997     

Relationship between photoperiod and secretion of the diapause hormone during larval stages of the silkworm, Bombyx mori L., reared on an artificial diet

The suboesophageal ganglion of the silkworm, Bombyx mori synthesizes sufficient diapause hormone to produce diapause eggs, regardless of the photoperiodic conditions experienced during the larval stages. When larvae destined to produce non-diapause eggs are implanted with the brain-suboesophageal ganglion complex from larvae which have been reared under short-day conditions, the resulting adults lay diapause eggs. The larvae receiving the complex from larvae reared under long-day conditions gave rise to adults which did not produce any diapause eggs. The brains from pupae which have been reared under long-day conditions show an activity inhibiting the secretion of diapause hormone by the suboesophageal ganglion. The mechanism through which the brain controls the secretion of diapause hormone from the suboesophageal ganglion can be modified by photoperiodic conditions during the larval stages.     

Summer dormancy ensures univoltinism in the predatory bug Picromerus bidens

The seasonal cycle of Picromerus bidens L. (Heteroptera: Pentatomidae) is usually considered to be univoltine with an obligatory winter egg diapause. Seasonal adaptations of the species were studied in the laboratory and in field experiments. When reared under short-day photoperiodic conditions (L12:D12 and L14:D10), all females began to lay eggs synchronously soon after their emergence. However, in the females reared under long-day conditions (L18:D6 and L20:D4) and outdoors in June–July, oviposition was significantly delayed. This delay in reproduction induced by photoperiodic conditions and then spontaneously terminated was considered to be aestivation. Egg batches laid by females in the laboratory and in the field were kept at 25 °C for two months. From 30.8 to 93.8% of batches contained eggs which hatched without cold treatment between day 14 and 60 after oviposition. The proportion of eggs hatched was 17.7 to 20.9% in the short-day regimes, while it was significantly less (5.7 to 6.0%) under long-day conditions. It is concluded that in some eggs diapause is of low intensity and that if under natural conditions the first batches had been laid at the end of June, nymphs would have hatched at least from some eggs during the same season even without cold treatment. Such untimely hatching would have resulted in the death of nymphs and adults unprepared for overwintering. A photoperiodic response which induces aestivation in the early emerging adults in June–August may prevent early oviposition and occurrence of a second generation and thus maintains univoltinism in P. bidens.     

Effects of compound eye-removal on the photoperiodic response of the band-legged ground cricket, Pteronemobius nigrofasciatus

The band-legged ground cricket Pteronemobius nigrofasciatus shows a clear photoperiodic response at 25°C with respect to the control of the induction of embryonic diapause. When crickets were reared under a short-day (LD 12 12) photoperiod and then transferred to a long-day (LD 16 8) photoperiod upon adult emergence, the adults mainly laid nondiapause eggs. However, adults maintained continuously under short-day conditions laid dispause eggs. When compound eyes were bilaterally removed after adult emergence, the crickets mainly laid nondiapause eggs, irrespective of the photoperiod. Thus, the adults completely lost their sensitivity to photoperiod after bilateral removal of their compound eyes. Unilateral removal of the compound eye also affected the crickets under a short-day photoperiod, and the incidence of diapause eggs was intermediate between that laid by intact adults and that laid by adults after the bilateral removal of compound eyes. The incidence of diapause eggs in sham-operated crickets was not significantly different from that in intact crickets under both sets of photoperiodic conditions. These results show that P. nigrofasciatus perceives the photoperiod through its compound eyes.     

Artificial selection for responsiveness to photoperiodic change alters the response to stationary photoperiods in maternal induction of egg diapause in the rice leaf bug Trigonotylus caelestialium

Female adults of the rice leaf bug Trigonotylus caelestialium (Kirkaldy) (Heteroptera: Miridae) produce non-diapause eggs under long-day conditions, whereas they produce diapause eggs under short-day conditions. These egg-production modes change following a photoperiodic change from long-day to short-day conditions or vice versa, with individual variations in responsiveness shown in the time from the photoperiodic change to the mode change. Strains of this insect with higher or lower responsiveness to photoperiodic change were established after several generations of selection, indicating that the individual variation has a genetic basis. The selected strains that were more responsive and less responsive to one photoperiodic change were found to be less responsive and more responsive to the opposite photoperiodic change, respectively, indicating a significant negative correlation between responsiveness to reciprocal photoperiodic changes. The selected strains also had a significantly different incidence of diapause-egg producers in stationary photoperiods compared to a non-selected strain, showing that selections for responsiveness to photoperiodic change were essentially the same as selections for a higher or lower incidence of diapause-egg producers. These results indicate that responsiveness to photoperiodic change is one aspect of the tendency to produce diapause or non-diapause eggs.     

Photoperiodic induction of the first and the second diapause in the bean bug,Riptortus clavatus: a photoperiodic history effect

Summary In nondiapause adults raised under a long-day photoperiod, the critical daylength for diapause induction was between 13 and 14 h although some individuals did not respond to the short-day photoperiod and went on laying eggs. In postdiapause adults in which LD 1311 induced the first diapause (L13 insects), the critical daylength for diapause reinduction was between 13 and 14 h, whereas it was between 12 and 13 h in postdiapause adults in which LD 1014 induced the first diapause (L10 insects). Under LD 1311, a small proportion of L10 insects went into the second diapause after great delay as compared with L13 insects. Under LD 1014, on the other hand, L10 insects went into the second diapause more rapidly than L13 insects. Therefore, the photoperiod which had induced the first diapause affected the photoperiodic induction of the second diapause not only in the critical daylength but also in the speed of response. In Riptortus clavatus, the photoperiodic history influences the subsequent photoperiodic response even after a physiological state induced by the previous photoperiod was terminated completely.Abbreviations L13 insects postdiapause adults in which LD 1311 induced the first diapause - L10 insects postdiapause adults in which LD 1014 induced the first diapause     

Diapause induction in the codling moth, Cydia pomonella: effect of prediapause temperatures

The effect of four prediapause temperatures (18, 22, 26 and 30°C) on the photoperiodic response of the codling moth, Cydia pomonella (L.), was studied under controlled conditions. The highest rates of diapause were recorded, for all day-lengths, at temperatures of 22 and 26°C while relatively lower rates of diapause were elicited at 18 and 30°C. The same trend was demonstrated by projecting the values of the critical photoperiod which induces 50% diapause (=CPhP₅₀) over the prediapause temperature. The change in diapause incidence as a function of photoperiod, at all prediapause temperatures, exhibited a response characteristic of long-day insects, i.e. high rates of diapause at short days (12–13.5 h) and a decrease in diapause incidence at long days (14–15 h). The results for temperatures 22, 26 and 30°C support the view that lower prediapause temperatures enhance diapause induction, at a give photoperiod, while higher temperatures tend to avert or diminish the process. On the other hand, the low rates of diapause obtained at 18°C contradict this view. Nevertheless, high correlation was found between the laboratory evidence and field data, indicating the adaptability of the Israeli codling moth to subtropical climate.     

Photoperiodic responses during larval development and diapause of two geographic ecotypes of the rice stem maggot, Chlorops oryzae

Chlorops oryzae is bivoltine in northern Japan but trivoltine in the southern part of the country. In the bivoltine strain, both the egg and larval stages were found to be sensitive to photoperiod. When the egg stage was exposed to a long-day photoperiod (16L:8D), larval development showed a short-day type response, and mature third-instar larvae entered a summer diapause under a long-day photoperiod (15L:9D). When eggs experienced short days, the first-instar larvae entered a winter diapause under short-day conditions, and the critical photoperiod in the larval stage ranged from about 14L:10D to about 12L:12D as the photoperiod experienced by the eggs increased from 12L:12D to 14L:10D. However, the development of the larvae after overwintering was not influenced by the photoperiod. In the trivoltine strain, larval development was retarded under a 14L:10D photoperiod but not under either shorter or longer photoperiods, when larvae had spent the egg stage under a 16L:8D photoperiod. The critical photoperiod of the larval stage for the induction of a winter diapause in the first instar was about 12L:12D, though it varied to some extent with the photoperiod during the egg stage. Thus, Chlorops oryzae was able to adapt itself to the local climatic conditions by the development of variable and complicated photoperiodic responses.     

Photoperiodic Control of Pre-Adult Development and Adult Diapause Induction in Zoophytophagous Bug Dicyphus errans (Wolff) (Heteroptera,Miridae)

Zoophytophagous plant bugs (Heteroptera, Miridae) increasingly attract interest as agents of biological plant protection. In the laboratory experiment, the effects of the day length and temperature on the duration of the pre-adult period and on induction of facultative winter adult diapause were studied in Dicyphus errans (Wolff, 1804) collected in Italy. The experiment demonstrated that at 20°C the duration of the pre-adult period of D. errans significantly depended on the day length. On average, females developed 1.3 days longer than males and, at the same time, the day length equally influenced the duration of the pre-adult period in both sexes. The pre-adult period was the shortest under short-day conditions (10 to 12 h of light per day), reached its maximum at day length of 14 h, but then decreased at 15 h, and at day length of 16 h it was as short as under short-day conditions. Also, a pronounced long-day type photoperiodic response of adult diapause induction was recorded in females of D. errans at 20°C: under short-day conditions (10 to 14 h of light per day) almost all females entered diapause, whereas under long-day conditions (15 and 16 h of light per day) about 90% of females were mature. The threshold of this photoperiodic response was close to 14 h 30 min. The mean (± S.D.) egg load of mature females was 6.3 ± 4.0 eggs per female and did not depend on the day length at which the female was reared before and after the final molt. When photoperiodic response of adult diapause induction was observed at two constant temperatures (20 and 25°C), the proportion of mature females depended significantly on the day length but not on the temperature: the shapes of the photoperiodic response curves of diapause induction were almost the same within the near-threshold zone at 20 and 25°C, i.e., the photoperiodic response was thermostable. The set of two photoperiodic responses manifested at different stages of the species’ life cycle has an obvious adaptive significance. In Central Europe, D. errans has 2 or 3 generations per year and hibernates at the adult stage. Due to the thermostable photoperiodic response, females enter diapause always at the same time at the end of summer, regardless of the weather conditions of a particular year. When oviposition and pre-adult development are extended over a prolonged period in summer, nymphs from the later eggs might not be able to molt to adults in due time and then fully prepare for stable winter diapause. Under such circumstances, the photoperiodic response controlling the rates of pre-adult development acquires apparent adaptive meaning: with an autumnal shortening of the day length to 10–12 h, even under conditions of seasonal decrease in temperature, the rates of nymphal development increase and, thus, the chances of nymphs from the later eggs to molt to adults and properly prepare for overwintering also increase. The new data should be taken into account when analyzing the seasonal cycle of D. errans and developing the programs of mass rearing of this zoophytophagous mirid as an agent of biological plant protection.

     

Regulation of adult diapause inCoccinella septempunctata septempunctata andC. septempunctata brucki from two regions of Japan (A Minireview)

In similar climatic conditions of central/northern Europe and Hokkaido, Japan, both subspecies ofCoccinella septempunctata L. have similar life-cycles: long-day photoperiodic response ensures the induction of winter diapause. In the mild climate of Honshu, Japan,C. s. brucki Mulsant shows a different life cycle: short-day photoperiodic response leads to the induction of summer diapause while overwintering is quiescence. All populations show an important variation in photoperiodic response.     

Insect circadian rhythms and photoperiodism

Two clock-controlled processes, overt circadian rhythmicity and the photoperiodic induction of diapause, are described in the blow fly,Calliphora vicina and the fruit fly,Drosophila melanogaster. Circadian locomotor rhythms of the adult flies reflect endogenous, self-sustained oscillations with a temperature compensated period. The free-running rhythms become synchronised (entrained) to daily light:dark cycles, but become arrhythmic in constant light above a certain intensity. Some flies show fragmented rhythms (internal desynchronisation) suggesting that overt rhythmicity is the product of a multioscillator (multicellular) system. Photoperiodic induction of larval diapause inC. vicina and of ovarian diapause inD. melanogaster is also based on the circadian system but seems, to involve a separate mechanism at both the molecular and neuronal levels. For both processes in both species, the compound eyes and ocelli are neither essential nor necessary for photic entrainment, and the circadian clock mechanism is not within the optic lobes. The central brain is the most likely site for both rhythm generation and extra-optic photoreception. InD. melanogaster, a group of lateral brain neurons has been identified as important circadian pacemaker cells, which are possibly also photo-sensitive. Similar lateral brain neurons, staining for arrestin, a protein in the phototransduction ‘cascade’ and a selective marker for photoreceptors in both vertebrates and invertebrates, have been identified inC. vicina. Much less is known about the cellular substrate of the photoperiodic mechanism, but this may involve thepars intercerebralis region of the mid-brain.     

Induction of adult diapause and of low and high reproductive states in a parasitoid wasp,Ooencyrtus nezarae, by photoperiod and temperature

Ooencyrtus nezarae Ishii (Hymenoptera: Encyrtidae) was reared on eggs ofRiptortus clavatus (Thunberg) (Heteroptera: Alydidae) at various temperatures under long-day (L16:D8) or short-day (L10:D14) conditions. There was no diapause during egg, larval or pupal stages under any set of conditions examined. However, at 15°C under short-day conditions, vitellogenesis was arrested in all adult females and they entered diapause. At 15°C under long-day conditions, or at 20°C under short-day conditions, some adult females entered diapause. Under the latter set of conditions, the adult females laid eggs but they laid fewer eggs than under long-day conditions, Even at 25°C, under short-day conditions, adult females laid fewer eggs than under long-day conditions, and this low rate of oviposition was attributed to the retarded development of ovaries. Diapause adults reared at 15°C were more resistant to low temperature than nondiapause adults reared at 25°C.     

Neurons important for the photoperiodic control of diapause in the bean bug, <Emphasis Type="Italic">Riptortus pedestris</Emphasis>

The morphology and functions of the brain neurons projecting to the retrocerebral complex were examined in terms of photoperiodic control of adult diapause in the bean bug, Riptortus pedestris. Backfills through the nervi corporis cardiaci stained 15-20 pairs of somata in the pars intercerebralis (PI) with contralateral axons, and 14-24 pairs in the pars lateralis (PL) with ipsilateral axons to the nervi corporis cardiaci. In the PL, two clusters of somata, PL-d and PL-v, were found. Forwardfills showed neurons in the PI terminated in the aorta, and those in the PL at the corpus cardiacum, corpus allatum, and aorta. Removal of the PI did not cause effects on diapause incidence both under short-day (12 h:12 h, light:dark) and long-day conditions (16 h:8 h, light:dark) at 25 degrees C. Under short-day conditions, diapause incidence was significantly lower than the controls after removal of the PL. Either removal of PL-d or PL-v did not reduce diapause incidence. It decreased only when both the PL-d and PL-v were ablated. The PI is not indispensable for diapause in R. pedestris, and both PL-d and PL-v neurons are suggested to be involved in photoperiodic inhibition of ovarian development.     

Expression of cytochrome c oxidase subunit 1 gene in the brain at an early stage in the termination of pupal diapause in the sweet potato hornworm, Agrius convolvuli

Suppression-subtractive hybridization was used to isolate cDNAs specifically expressed in the brain at the termination of pupal diapause in Agriusconvolvuli. One of the isolated clones shows similarity to the cytochrome c oxidase subunit 1 (COX1) gene. The full-length cDNA was obtained from brain mRNA by rapid amplification of cDNA ends (RACE). The insert is 1.65 kb in length and has an open reading frame of 1.46 kb which encodes a putative protein of 486 amino acid residues. RT-PCR reveals that the mRNA increases dramatically at an early stage of diapause termination. Activity of cytochrome c oxidase in the brain also increases at the same time. The up-regulation of this gene suggests that expression of the COX1 gene and ATP synthesis are initiated in the brain in association with diapause termination.