Diapause‐inducing signals prolong nymphal development in the two‐spotted spider mite Tetranychus urticae

Female two‐spotted spider mite Tetranychus urticae are grown under different photoperiods and the photoperiodic regulation of diapause is examined. The photoperiodic response curve for diapause induction was of the long day–short day type, with critical day lengths (CDLs) of 2 and 12.5 h; diapause was induced between these CDLs. The preimaginal period is significantly longer in diapausing females than in non‐diapausing females; moreover, a significant positive correlation is detected between diapause incidence and deutonymphal period. Diapause incidence is high when long‐night photoperiods are applied against a background of continuous darkness in the stages including the deutonymph; this stage appears to be the most sensitive to photoperiod. These observations suggest that diapause‐inducing conditions inhibit nymphal development, particularly in the deutonymphal stage when photoperiodic time measurement for determination of reproduction or diapause is carried out.     

Effects of photoperiod and temperature on diapause induction in Conogethes punctiferalis (Lepidoptera: Pyralidae)

The yellow peach moth, Conogethes punctiferalis (Guenée), a multivoltine species that overwinters as diapausing larvae, is one of the most serious insect pests on maize in China. Effect of photoperiod and temperature on larval diapause was examined under empirical laboratory conditions. Short‐day treatments caused larval diapause at 25°C, and the critical photoperiod was between 12 and 13 h (or 12 h 51 min) light per day. No sensitive instar was identified for diapause induction under alternated short‐ (L : D 11 : 13 h) and long‐day (L : D 14 : 10 h) treatments at different larval stages. However, accumulative treatment of three instars and 10 d under short‐day treatment was required for the induction of 50% larval diapause. All larvae entered diapause at 20°C, whereas less than 3% did so at 30°C, irrespective of the long‐ or short‐day treatment. Furthermore, under the short‐day treatment, more than 90% of larvae went into diapause with temperatures ≤ 25°C, but less than 17% did so at 28°C. In contrast, under the long‐day treatment, less than 19% of larvae went into diapause with temperatures ≥ 23°C. The forward shift (5°C) of critical temperature under the long‐day regime demonstrated the compensatory effect of temperature and photoperiod on diapause induction. In conclusion, C. punctiferalis had a temperature‐dependent type I photoperiodic diapause response; there was no sensitive instar for diapause determination, but the photoperiodic accumulation time countermeasures both of the short‐day cycles and the number of instars exposed, and the photoperiodic diapause response, was a temperature‐compensated phenomenon.     

Timing of diapause induction and its life‐history consequences in Nezara viridula: is it costly to expand the distribution range?

Abstract. 1. From the early 1960s to 2000 Nezara viridula (Heteroptera: Pentatomidae) expanded its range northwards in Japan and reached Osaka following climate warming recorded in the region. 2. The timing of diapause induction and its effect on life‐history traits were studied under quasi‐natural conditions in Osaka. Egg masses were placed outdoors in six series in July–November 1999. Developmental events were monitored until September 2000. 3. Adult diapause was induced in September–October in agreement with the photoperiodic response obtained under laboratory conditions. Induction of diapause in early October ensured the highest winter survival. Nymphs that hatched after late September died by December–April showing that the species cannot survive winter in the nymphal stage. 4. Life‐history traits varied between the early (non‐diapause reproduction) and late (post‐diapause reproduction) series. Thus, non‐diapause females produced significantly fewer egg masses than did females that reproduced only after diapause. The timing of diapause induction strongly affected overwintering success and post‐diapause performance: females that became adults and entered diapause in October lived longer, had a longer period of oviposition, and produced more eggs in larger egg masses than females that attained adulthood and entered diapause in September. 5. Females from the early series reproduced until late November, although progeny from the late September eggs were destined to die during the winter. Pre‐winter reproduction of adults that emerged in mid‐September or later was a result of the imperfect timing of diapause induction. It is an ineffective allocation of resources and may be considered the ecological cost of range expansion. 6. To establish in the region, N. viridula will probably evolve a lengthening of the critical photoperiod of the diapause induction response. This will allow the species to enter diapause earlier and, thus, avoid maladaptive late‐autumn reproduction but, perhaps, increase the cost of diapause because of a possible adverse impact of pre‐winter high temperature conditions on overwintering.     

Effects of photoperiod and temperature on reproductive diapause in Ophraella communa (Coleoptera: Chrysomelidae), a potential biocontrol agent against Ambrosia artemisiifolia

Abstract To investigate the seasonal adaptation strategies of Ophraella communa to new habitats, the effects and regulation mechanisms of photoperiod and temperature on the reproductive diapause in a population collected from Changsha, Hunan were examined. Adults showed obvious reproductive diapause, which was regulated by photoperiod and temperature. At 30°C, there was no adult diapause occurring under either long‐day or short‐day conditions; at 25°C the pre‐oviposition period was short and fecundity was high in adult females under L : D 16 : 8 h, whereas under L : D 12 : 12 h, a few females entered reproductive diapause; at 20°C under short‐day conditions, all female adults entered diapause. The pre‐oviposition period was significantly prolonged when the pupae and adults were transferred from long‐days to short‐days, but the day length influence was not obvious when they were transferred only in the adult stage. However, the fecundity dropped greatly no matter whether the photoperiod shifted to short‐days only in the adult stage or whether the shift occurred in both the pupal and adult stage. The fecundity was extremely low when photoperiod shifted from long‐days to short‐days in both pupal and adult stages. This was an indication that the pupal and adult stages were the photoperiod‐sensitive stage for adult reproductive diapause. This was especially true for the photoperiod in the pupal stage, which has a distinctly significant regulative effect on reproductive diapause. Additionally, this article also addresses the reason for different photoperiodic response patterns in reproductive diapause induction between the Changsha strain and the Tsukuba strain (Japan) of O. communa.     

Responses to stepwise photoperiodic changes for the larval diapause of the Indian meal moth Plodia interpunctella

Abstract The Indian meal moth Plodia interpunctella Hübner (Lepidoptera: Pyralidae) diapauses as a last‐instar (fifth) larva. At 30 °C, no larvae enter diapause under any photoperiodic conditions; at 25 °C, the photoperiodic response curve is a long‐day type with a critical length of approximately 13 h light; at 20 °C, diapause is induced moderately even under long days (> 13 h). Cumulative effects of short days or long days on diapause induction are determined by alternate, stepwise and gradually changing regimes of photoperiod at 25 °C. When the larvae are repeatedly exposed to LD 16 : 8 h and LD 12 : 12 h photoperiods every other day, the incidence of diapause is 37%. When the larvae are placed under an LD 16 : 8 h photoperiod for 2 days and then under an LD 12 : 12 h photoperiod for 1 day, it is 38 %. Exposure to an LD 16 : 8 h photoperiod for 1 day and then to an LD 12 : 12 h photoperiod for 2 days induces only 15% diapause. This may indicate that the photoperiodic information is not accumulated in a simple fashion despite the generally accepted hypothesis (i.e. photoperiodic counter). Larvae exposed to an LD 16 : 8 h photoperiod for 5 days after oviposition express a very high incidence of diapause even under short days between an LD 2 : 22 h and LD 12 : 12 h photoperiod. After 10 days exposure to an LD 16 : 8 h photoperiod, however, the short day does not induce diapause strongly. On the other hand, an LD 12 : 12 h photoperiod in the early larval life is highly effective in the induction of diapause. A gradual increase or decrease of photoperiod (2 min day^?1) shows that the direction of photoperiodic change does not affect the diapause determination.     

Photoperiodic induction of prepupal diapause and its role in synchronization with host phenology in the hibiscus caterpillar,Xanthodes transversa

The hibiscus caterpillar, Xanthodes transversa (Lepidoptera: Noctuidae), is a multivoltine insect that is an important pest of Malvaceae plants such as the okra, Abelmoschus esculentus, and the common rose mallow, Hibiscus mutabilis, in Japan. In the present study, the effects of photoperiod and temperature on the induction of prepupal diapause and the adaptive significance of this diapause were examined in a local population of X. transversa in Miyazaki, Kyushu, southwestern Japan. Larvae showed a long‐day photoperiodic response for controlling the induction of prepupal diapause with a critical day length between 13 and 14 h at 20 to 25°C. Under long‐day conditions larvae rapidly pupated from the sixth instar, but under short‐day conditions they entered diapause in the prepupal stage. Diapause occurrence in the field increased in late September, which was consistent with the laboratory results in terms of the photoperiodic response. Non‐diapause development after this time is maladaptive because most larvae of the next generation could not reach the critical stage (prepupae) before winter and died during early winter in outdoor experiments. Larvae suffered from a high rate of mortality when fed leaves collected late in autumn. The photoperiodic response for controlling the induction of diapause in this insect may play an important role in synchronizing the life cycle with the seasonal changes in food and temperature conditions.     

Effects of diet, photoperiod and temperature on the postdiapause reproduction in the cabbage bug,Eurydema rugosa

InEurydema rugosa Motschulsky (Heteroptera: Pentatomidae), the type of food supplied (i.e. seeds or leaves of the brown mustard,Brassica juncea Hemsel) and photoperiod, which control the induction of adult diapause, do not play a role in the initiation of reproduction after overwintering. A temperature above 13.2°C was required to start reproduction. After its initiation, however, short-day conditions on seeds induced diapause again in some adults. Although a diet of seeds under long-day conditions, in common with short-day conditions, induced diapause in young adults (Numata & Yamamoto, 1990), it did not reinduce diapause in adults after overwintering. Thus,E. rugosa that had overwintered became sensitive to diapause-inducing photoperiod again but not to dietary factors.     

First evidence for photoperiodic regulation of the life cycle in a millipede species, Polydesmus angustus (Diplopoda: Polydesmidae)

The hypothesis that the periods of dormancy previously described in the millipede Polydesmus angustus may be photoperiodically induced diapauses was tested experimentally. In this species, biennial individuals exhibit two successive periods of dormancy: aestivation in the penultimate stadium (stadium VII) and reproductive dormancy in the adults, which emerge in autumn. It was first established that the reproductive dormancy is not a thermally controlled state of quiescence. When adults emerging in autumn were kept at 16 °C under natural photoperiod, their reproduction was delayed for several months in comparison with adults emerging in spring at similar temperatures. This indicates that the reproductive dormancy begins with a period of diapause. Further experiments provided evidence of a photoperiodic induction of the adult diapause. When millipedes were reared under short day length (L:D 12:12 h) throughout their development, they required more time to reproduce than millipedes reared under long day length (L:D 16:8 h) at the same temperatures. Photoperiod influenced reproduction in females, but no significant effects were detected in adult males. On the other hand, stadium VII was markedly longer at L:D 16:8 h than at L:D 12:12 h in both sexes, which strongly suggests that aestivation is also induced by photoperiod. However, the effects on the duration of stadium VII varied among individuals, some of which showed no response to long days. This study is the first to document photoperiodic regulation of the life cycle in the class Diplopoda, a trait common in other classes of terrestrial arthropods.     

Maternal influence on diapause induction in Trichogramma (Hymenoptera: Trichogrammatidae): the dynamics of photosensitivity

It is known that the prepupal diapause in Trichogramma is dependent on temperature conditions of embryonic and larval development and on the photoperiodic conditions of preimaginal development of maternal females. However, the relative photosensitivity of different preimaginal stages has been never investigated. We studied the position of the photosensitive period over the preimaginal development of maternal females in T. embryophagum Htg. and T. principium Sug. et Sor. by transferring preimaginal stages between diapause‐averting ‘long’ day (L : D = 20 : 4) and diapause‐inducing ‘short’ day (L : D = 12 : 12). Results showed that the influence of maternal photoperiod on progeny diapause was determined during the late pupal stage (last days of preimaginal development at 20°C). During this time, the critical duration of the photoperiodic induction was extremely small: one short or long day caused almost the same effect as the permanent development under these conditions. As a whole, photoperiodic response in Trichogramma was found to be unusually rapid, labile and easily reversible which is probably explained by extremely small size and fast development of these egg parasitoids. The results of this study could be used for elaboration of optimal methods for Trichogramma mass rearing and storage and for prediction of its seasonal cycles under natural conditions.     

Genetic analysis of diapause capability and association between larval and pupal photoperiodic responses in the flesh fly Sarcophaga similis

Abstract A variant of the flesh fly Sarcophaga similis, which does not enter pupal diapause even under diapause‐inducing conditions, is established by artificial selection. Interline crosses of the wild‐type and the variant revealed that the diapause capability is inherited in an incomplete dominant manner. Neither sex linkage nor a maternal factor is involved in the mode of inheritance. Genetic and genetic–environmental interactions are involved in the induction of diapause. In the wild‐type, the post‐feeding larval period is prolonged in response to short days. However, in the variant, the duration of the larval period under short‐day conditions is identical to that under long‐day conditions. Long‐day responses under short‐day conditions at both the larval and pupal stages in the variant indicate that the responses are established by common factors in both stages. The factors causing the long‐day responses under short‐day conditions at different developmental stages in the variant remain to be identified. However, it is plausible to hypothesize that common factors regulate ecdysteroid release at both the larval and pupal stages, and that malfunction of the system regulating these factors triggers such ecdysteroid release, irrespective of the photoperiod. Hence, the photoperiodic responses disappear in the variant in both stages. The adult stage of the variant has a functional circadian clock, suggesting that the nondiapause phenotype is not necessarily involved in malfunction of the circadian clock.     

European hamsters (Cricetus cricetus) show a transient phase of insensitivity to long photoperiods after gonadal regression

Annual rhythms of body weight and reproduction in the European hamster (Cricetus cricetus) are the result of an interaction between seasonal changes in day length (photoperiod) and seasonal changes in the responsiveness of animals to these photoperiods. The present study demonstrates that under natural conditions European hamsters are not able to perceive long photoperiods (i.e., a 16L:8D cycle) before mid-November. This is an important difference to other hamster species, in which regrowth of the gonads can be stimulated by exposure to long photoperiods at any stage of gonadal regression. The experiments also demonstrate the existence of an annual phase of sensitivity to long photoperiods that starts around mid-November and extends until March/April. During this phase of sensitivity, exposure to a long photoperiod (16L:8D) induced gonadal regrowth within 3 wk. Additional experiments with an accelerated photoperiodic lighting regimen indicated that a photoperiod of approximately 13 h is necessary to stimulate gonadal regrowth. Under natural light conditions in Stuttgart (48.46 degrees N), a photoperiod of 13 h is reached by the beginning of April, which fits well with the finding that the majority of animals kept under a natural light:dark cycle had well-developed gonads by the end of April. Nevertheless, these animals showed a rather variable timing of gonadal regrowth, ranging from early January to late April. This is most likely the result of two processes: first, an endogenous mechanism (photorefractoriness) that induces gonadal recrudescence without any photoperiodic information while the animals are still in their hibernation burrows, and second, a direct stimulatory effect of long photoperiods.     

Effects of temperature,photoperiod and soil humidity on induction of pseudopupal diapause in the bean blister beetle Epicauta gorhami

Larvae of the bean blister beetle Epicauta gorhami Marseul (Coleoptera: Meloidae) feed on grasshopper eggs in soil and undergo hypermetamorphosis. This beetle undergoes larval diapause in the fifth instar as a pseudopupa, a form characteristic of hypermetamorphosis in meloid beetles. The effects of temperature, photoperiod and soil humidity on larval development of E. gorhami are examined in a population in Miyazaki, Japan, using egg pods of Locusta migratoria L. as food. At lower temperatures (20 and 22.5 °C), all larvae become pseudopupae, regardless of the photoperiod. By contrast, at higher temperatures (27.5 and 30 °C), almost all larvae pupate at the end of the fourth instar, again regardless of the photoperiod. A long‐day photoperiodic response occurs only at an intermediate temperature (25 °C): under an LD 12 : 12 h photocycle, all larvae enter diapause, although the diapause incidence tends to decrease as the day length becomes longer. Pseudopupae are immobile and remain in diapause for ≥120 days when they are kept under the same conditions, except that diapause terminates within a relatively short time at 30 °C. Although lower soil humidity retards post‐feeding development, soil humidity has no effect on the diapause incidence. On the basis of the short developmental period and diapause avoidance under summer conditions, it is suggested that this beetle partially produces two generations a year in southwestern Japan.     

Photoperiodic response in the subtropical and warm‐temperate zone populations of the southern green stink bug Nezara viridula: why does it not fit the common latitudinal trend?

The photoperiodic response of diapause induction is studied in females of five subtropical and warm‐temperate zone populations of Nezara viridula (L.) (Heteroptera: Pentatomidae) in Japan (26.4–34.7°N; 127.4–135.7°E). Laboratory tests at 25 °C demonstrate that both warm‐temperate and subtropical populations have pronounced photoperiodic responses of adult diapause induction. Under short‐day conditions (LD 10 : 14 h), 73–100% of females enter diapause, whereas, under long‐day conditions (LD 15 : 9 h), 87–100% of females are nondiapause and reproduce. When the critical photoperiod for diapause induction is plotted against the latitude of origin of each population, the data points do not show the expected tendency of increasing critical photoperiod northwards but, instead, vary between 12 h 15 min and 13 h 30 min. It is suggested that adults from different populations of such a highly migratory species move often among subtropical islands (by themselves or being assisted by typhoons), thus constantly destabilizing the photoperiodic responses. Although important for general synchronization of seasonal development in the tropics and subtropics, winter diapause might not be so critical for survival in mild winters in these zones. Such circumstances might make the selective pressure over the photoperiodic response less severe in the tropics and subtropics than in the temperate zone. It is suggested that the current climate warming might contribute to this situation as well by promoting polewards migrations and lessening the selective pressure of overwintering conditions.     

Diapause decision in the small tortoiseshell butterfly,Aglais urticae

Insects in temperate areas spend the inhospitable winter conditions in a resting stage known as diapause. In species that diapause in the larval or pupal stage, the decision whether to diapause or develop directly is customarily taken during the late instars, with long days (i.e., long light phases) and high temperatures promoting direct development. Among butterflies that overwinter as adults, data are rare and variable, but imply that the larval daylength conditions can affect the pathway decision. We studied the small tortoiseshell, Aglais urticae L. (Lepidoptera: Nymphalidae, Nymphalini), which is partially bivoltine from Central Scandinavia and southwards, and tested whether the pathway decision is taken in the larval or adult stage. We reared larvae under long‐day (L22:D2) or short‐day (L12:D12) photoperiods, and recorded the pathway taken by the eclosing adults by scoring their propensity to mate and produce eggs. We also tested whether the larval photoperiod influenced adult ability to diapause by assessing adult survival. The results clearly indicate that (1) there is no detectable effect of larval photoperiod treatment on the pathway decision taken by adults whether to enter diapause or to develop directly, (2) some individuals are obligately univoltine and insensitive to photoperiod during adulthood, whereas (3) other individuals can facultatively enter diapause or direct development, depending on the photoperiod experienced after adult eclosion.     

Effect of photoperiod and allatectomy on reproduction and (second) diapause induction in post-diapause adult females of the Colorado potato beetle,Leptinotarsa decemlineata Say

Summary

The effect of photoperiod and allatectomy on the rates of oviposition and juvenile hormone (JH) synthesis was studied in female beetles after the break of adult diapause. The results indicate that after diapause, photoperiod has no effect on oviposition rates. However, the photoperiodic effect on diapause induction is restored within a few days after the break of the first diapause. Allatectomy performed within one day after diapause did not induce a second diapause, whereas about 40% of the beetles allatectomized after 3 or more days responded by entering a second diapause. Oogenesis in the operated animals was never completely prevented under long and short day conditions. These preliminary results suggest a change in the sensitivity of post-diapause beetles to photoperiodic and endocrine manipulation as compared with pre-diapause insects.     

Intermittent character of adult diapause in Aelia acuminata (Heteroptera)

The response to photoperiod of field-collected Aelia acuminata was studied by exposing insects to three photoperiodic regimes. After the completion of diapause the insects do not respond to photoperiod: in mid-February the length of the pre-oviposition period is the same under both long and short photoperiods. After the onset of oviposition, insects again become responsive to photoperiod regardless of the time of year: under long day, oviposition lasts until death, whereas under short day the females cease oviposition after about 3 weeks. After a further 2 or 3 months without ovipositing, these females which are still experiencing short-day conditions resume reproduction for a further 4–7 weeks and long-lived individuals have three oviposition periods. A regulatory mechanism is suggested for the alternation between oviposition and diapause.     

Melatonin pathway transmits information to terminate pupal diapause in the Chinese oak silkmoth Antheraea pernyi and through reciprocated inhibition of dopamine pathway functions as a photoperiodic counter

The present study investigated the functional involvement of melatonin and dopamine in photoperiodism to terminate pupal diapause in the Chinese oak silkmoth, Antheraea pernyi (Lepidoptera: Saturniidae). Diapause in this long‐day (short‐night) species is maintained during long nights and can be terminated by exposure to a short‐night photoperiod. We observed the effects of melatonin and dopamine and their receptor antagonists on diapause pupae. Melatonin and flupentixol, a dopamine receptor antagonist, terminated pupal diapause even under long‐night photoperiods. Dopamine and luzindole, a melatonin receptor antagonist, retarded adult emergence during short nights, whereas melatonin advanced the timing of adult emergence under the short‐night photoperiod in a manner dependent on the number of injections. The results of the day‐length extension experiment indicated that a change in the photoperiod was immediately detected as mRNA expression of the rate‐limiting enzyme of melatonin production. These findings suggest that the melatonin pathway transmits information on the photoperiod to terminate the pupal diapause of A. pernyi. The melatonin pathway also inhibited the dopamine production system, and the dopamine pathway inhibited the melatonin production system. We propose an insect model of the photoperiodic counter driven by mutual inhibition between the melatonin and dopamine pathways.     

Inheritance of photoperiodic induction of larval diapause in the Asian corn borer Ostrinia furnacalis

The Asian corn borer Ostrinia furnacalis (Guenée) enters facultative diapause as fully‐developed larvae in response to short‐day conditions. As a consequence of geographical variation in photoperiodic response, moths from Nanchang (28°46′N, 115°50′E) enter diapause in response to short day‐lengths (D strain), even at the high temperatures whereas moths from Ledong (18°47′N, 108°89′E) exhibit almost no diapause under the same conditions (N strain). In the present study, crosses between the two strains are used to evaluate the inheritance of diapause under different photoperiods at temperatures of 22, 25 and 28 °C. The moths, both reciprocal crosses and backcrosses, show a clear long‐day response, similar to that of the D strain, suggesting that the photoperiodic response controlling diapause in this moth is heritable. However, the critical day‐length for induction of diapause is shorter in hybrids than in the D strain. The N strain also shows a short‐day photoperiodic response at the lower temperature of 22 °C, indicating that the N strain still has the capacity to enter a photoperiodically‐induced diapause, depending on the rearing temperature. The incidence of diapause in all crosses is highest with D strain fathers or grandfathers and lowest with N strain fathers or grandfathers, indicating that the male parent has significantly more influence on the incidence of diapause of subsequent progeny than the female. The results obtained from all crosses under LD 12 : 12 h or LD 13 : 11 h photocycles at 25 °C show that inheritance of diapause in O. furnacalis does not fit an additive hypothesis and that the capacity for diapause is transmitted genetically in the manner of incomplete dominance.     

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.