Diapause Termination Research Articles

Effect of photoperiod and temperature on reproductive diapause of Scotinophara lurida (Burmeister) (Heteroptera: Pentatomidae)

This study was carried out to investigate the effects of photoperiod and temperature on induction and termination of reproductive diapause in the black rice bug, Scotinophara lurida (Burmeister). Newly ecdysed fourth-instar nymphs and emerged adults of S. lurida adults did not enter reproductive diapause when reared at 30 °C in any photoperiod used. However, they exhibited the threshold photoperiod between 9 and 10 h at 25 °C and between 12 and 16 h at 20 °C adults overwinter in a state of reproductive diapause induced by short photoperiod and/or low temperature.

Factors affecting the natural duration of diapause and post-diapause development in the Mediterranean corn borer Sesamia nonagrioides (Lepidoptera: Noctuidae)

Sesamia nonagrioides responds to photoperiod for diapause termination at high temperature with a Type II response curve, and only photoperiods longer than 12:12 terminate diapause. However, these photoperiods never occur in the field when diapausing larvae are competent to terminate diapause. Under a temperature similar to the natural field temperatures diapause terminates spontaneously in approximately 4 months, which ensures that the larvae reach the middle of winter without pupation. S. nonagrioides larvae pupate after going through a specific number of light–dark cycles or days: the required day number (RDN) for diapause completion. This RDN could be modulated by temperature but more research is necessary to clarify this point. In post-diapause development, when a suitable temperature threshold is considered, the absolute accumulation of heat is more important than whether the temperature received is fluctuating or constant. The temperature threshold for diapause and post-diapause development was lower than the temperature threshold of larvae in continuous development. This is important for adjusting phenological models in S. nonagrioides and in other species, and may explain why in many cases adults appear in the field when the supposed temperature threshold for development has not been attained.

Characteristic Expression of Three Heat Shock-Responsive Genes During Larval Diapause in the Bamboo Borer Omphisa fuscidentalis

Three heat shock-responsive genes, Ofhsp70, Ofhsc70, and Ofhsp90, were identified in Omphisa fuscidentalis. These genes encode proteins with molecular weights of 70, 72, and 82 kDa, respectively, and were upregulated during heat shock. Ofhsp70 was expressed actively in the pre-diapause period, but its expression was low during diapause. While Ofhsc70 expression was low during pre-diapause and the first half of diapause, its expression increased greatly in the second half before diapause termination. In contrast, Ofhsp90 expression decreased by half during the transition to diapause and conspicuously decreased during late diapause. The results suggest that Ofhsp90 is associated with the maintenance of diapause and Ofhsc70 with the termination of diapause, whereas the expression of Ofhsp70 is unrelated to diapause. The insect molting hormone 20-hydroxyecdysone (20E) and juvenile hormone analog (JHA) caused increases in the mRNA expression of Ofhsc70, but not Ofhsp70 or Ofhsp90, in diapausing larvae. These transcriptional responses to 20E are consistent with the changes in ecdysteroid titer in the hemolymph relative to gene expression during diapause.

Historical and projected interactions between climate change and insect voltinism in a multivoltine species

AbstractClimate change can cause major changes to the dynamics of individual species and to those communities in which they interact. One effect of increasing temperatures is on insect voltinism, with the logical assumption that increases in surface temperatures would permit multivoltine species to increase the number of generations per year. Though insect development is primarily driven by temperature, most multivoltine insect species rely on photoperiodic cues, which do not change from year‐to‐year or in response to climate warming, to initiate diapause. Thus, the relationship between climate change and voltinism could be complex. We use a phenology model for grape berry moth, Paralobesia viteana (Clemens), which incorporates temperature‐dependent development and diapause termination, and photoperiod‐dependent diapause induction, to explore historical patterns in year‐to‐year voltinism fluctuations. We then extend this model to predict voltinism under varying scenarios of climate change to show the importance of both the quality and quantity of accumulated heat units. We also illustrate that increases in mean surface temperatures > 2 °C can have dramatic effects on insect voltinism by causing a shift in the ovipositional period that currently is subject to diapause‐inducing photoperiods.

A comparison of photoperiodic control of diapause between aestivation and hibernation in the cabbage butterfly Pieris melete

In the cabbage butterfly, Pieris melete, summer and winter diapause are induced principally by long and short daylengths, respectively; the intermediate daylengths (12–13h) permit pupae to develop without diapause. In this study, photoperiodic control of summer and winter diapause was systematically investigated in this butterfly by examining the photoperiodic response, the number of days required to induce 50% summer and winter diapause and the duration of diapausing pupae induced under different photoperiods. Photoperiodic response curves at 18 and 20°C showed that all pupae entered winter diapause at short daylengths (8–11h), the incidence of diapause dropped to 82.3–85.5% at 22°C without showing a significant difference between short daylengths, whereas the incidence of summer diapause induced by different long daylengths (14–18h) was varied and was obviously affected by temperature. By transferring from various short daylengths (LD 8:16, LD 9:15, LD 10:14 and LD 11:13) to an intermediate daylength (LD 12.5:11.5) at different times after hatching, the number of cycles required to induce 50% winter diapause (7.28 at LD 8:16, 7.16 at LD 9:15, 7.60 at LD 10:14 and 6.94 at LD 11:13) showed no significant difference, whereas by transferring from various long daylengths (LD 14:10, LD 15:9, LD 16:8 and LD 17:7) to an intermediate daylength (LD 12.5:11.5) at different times, the number of cycles required to induce 50% summer diapause (5.95 at LD 14:10, 8.02 at LD 15:9, 6.80 at LD 16:8, 7.64 at LD 17:7) were significantly different. The intensity of winter diapause induced under different short daylengths (LD 8:16, LD 9:15, LD 10:14 and LD 11:13) was not significantly different with an average diapause duration of 87 days at a constant temperature of 20°C and 92 days at a mean daily temperature of 19.0°C, whereas the intensity of summer diapause induced under different long daylengths (LD 14:10, LD 15:9, LD 16:8 and LD 17:7) was significantly different (the diapause duration ranged from 75 to 86 days at a constant temperature of 20°C and from 76 to 88 days at a mean daily temperature of 19.0°C).All results suggested that photoperiodic control of diapause induction and termination is significantly different between aestivation and hibernation.

Seasonal development of wheat midge, Sitodiplosis mosellana (Géhin) (Diptera: Cecidomyiidae), in Saskatchewan, Canada

Wheat midge, Sitodiplosis mosellana (Géhin) (Diptera: Cecidomyiidae), was first detected as early as 1901 in western Canada. The first major outbreak in Saskatchewan was recorded in 1983. In 1984, Saskatchewan wheat midge populations were found to be parasitized by the egg parasitoid, Macroglenes penetrans (Kirby) (Hymenoptera: Pteromálidae). This paper describes the effect of temperature on diapause termination, larval and pupal development, and on emergence of field populations of adult wheat midge, S. mosellana, and its parasitoid, M. penetrans, in Saskatchewan. Wheat midge and parasitoid populations were investigated from 1984 to 1985 in five wheat fields where wheat midge populations ranged from 5256 to 43,798 larvae/m 2. The appearance of midge larvae in soil samples on May 14 and May 9 in 1984 and 1985, respectively, marked the end of overwintering diapause. Pupae first appeared in samples on June 15 (139 degree-days (DD); >6 °C) and June 10 (125 DD) in 1984 and 1985, respectively. Adult midge and parasitoids began to emerge at all locations on July 6 (411 DD; >6 °C) and on July 9 (447 DD) in 1984 and 1985, respectively. In relation to the pest–host plant synchrony, adults of both wheat midge and parasitoids were present throughout July, with peak midge emergence coinciding both years with the emergence of primary wheat heads from the boot. We observed the first primary heads from about July 12 to 15 at the five sites. Therefore, the relatively long wheat midge emergence has significance because it contributes to damage on the first and second tillers and to a possible increase in populations for the following year. The use of temperature and day-degree accumulation in relation to development is discussed as a predictive tool for management decisions.

Diapause hormone in the corn earworm, Helicoverpa zea: Optimum temperature for activity, structure–activity relationships, and efficacy in accelerating flesh fly pupariation

Diapause hormone (DH) effectively terminated pupal diapause in Helicoverpa zea. This effect was temperature-dependent, with an optimum of 21 °C. The dose–response curve indicated an ED 50 of DH for diapause termination of approximately 100 pmol. The core sequence and essential amino acids were determined by bioassays using modified and truncated DH analogs. A C-terminal hepta-peptide, LWFGPRLa, was the core sequence required for diapause termination. Activity was lost when Alanine was substituted for any of the amino acids in the hepta-peptide, with the exception of Glycine. A fragment series of analogs suggested that the amide and Arginine were the most important components needed for terminating diapause. Leucine, Tryptophan, and Phenylalanine at the N-terminus of the hepta-peptide were also critical for activity. The C-terminal Leucine was less important: deletion resulted in decreased activity, although it could not be substituted by Alanine. The fact that a portion of the DH sequence is similar to the pyrokinin that accelerates fly pupariation prompted us to also evaluate the capability of DH to accelerate development in the flesh fly, Sarcophaga bullata. The threshold dose of DH essential to accelerate fly pupariation was 5 pmol for immobilization/retraction and longitudinal contraction and 10 pmol for tanning, approximately one or two orders of magnitude lower than the effective dose required for diapause termination in H. zea. Tensiometric measurements revealed that DH affected neuromuscular patterns of pupariation behavior and associated cuticular changes in a manner similar to that of the fly pyrokinins and their analogs.

Influence of temperature and darkness on embryonic diapause termination in dormant Artemia cysts that have never been desiccated

Environmental cues for embryonic diapause termination (EDT) were investigated in the laboratory-produced encysted dormant embryos of the brine shrimp, Artemia franciscana. The cysts were spawned and kept throughout in a 2% sea salt solution. They were activated by various temperatures of the temperate zones or by continuous dark condition (DD), resulting in a state of EDT, and were thereafter able to resume their subsequent development and hatch under appropriate conditions. The level of EDT was conveniently assayed by a hatch test observed within 2 days at 28 degrees C under continuous light condition (LL). A cold treatment of the newly spawned dormant cysts, at 4 degrees C under DD for more than 100 days, resulted in more than 95% hatch of the dormant cysts. Similar treatments of the dormant cysts but at room temperature or 28 degrees C led to significantly different results (30-40% hatch). Almost all the residual non-hatched cysts derived from the above could hatch after an additional cold treatment (at 4 degrees C under DD for about 100 days). This might prove to be latent partial bivoltine in Artemia. Meanwhile, a rearing condition (28 degrees C under LL) induced the newly spawned cysts to hatch scatteredly at and after 1 month, resulting in 22% cumulative hatch on the 92nd day after spawning. When the newly spawned dormant cysts were pretreated at 28 degrees C under DD for 5 or 14 days and then reared at 28 degrees C under LL, the cumulative hatch significantly increased (60%). These results are discussed with respect to probable diapause regulator(s) involved in EDT.

Temperature-Dependent Regulation of Reproduction in the Diving Beetle Dytiscus sharpi (Coleoptera: Dytiscidae)

The effects of temperature on the mating behavior, gonad development, germ cell maturation, and egg spawning of the predaceous diving beetle Dytiscus sharpi (Coleoptera; Dytiscidae), were investigated. By field observations, we found that mating behavior started in October and occurred more frequently from November to December. Under our laboratory breeding conditions, we observed almost the same seasonal variation in mating behavior. We found that temperatures lower than 20 degrees C were required to trigger mating behavior. We also found the same temperature threshold triggered gonadogenesis as well as spermatogenesis. Furthermore, for females, exposure to lower temperatures (<8 degrees C) during the winter was required for egg maturation and spawning in spring; that is, there was a second threshold for successful female reproduction. We conclude that the termination of summer reproductive diapause of D. sharpi is regulated in a temperature-dependent manner, thus effecting the adaptation of D. sharpi to southern warm habitats.

Host plant and latitude‐related diapause variation in Rhagoletis pomonella: a test for multifaceted life history adaptation on different stages of diapause development

Variation in the overwintering pupal diapause of Rhagoletis pomonella appears to adapt sympatric populations of the fly to seasonal differences in the fruiting times of their host plants, generating ecological reproductive isolation. Here, we investigate what aspects of diapause development are differentially affected (1) by comparing the propensities of apple vs. hawthorn-infesting host races of R. pomonella to forgo an initially deep diapause and directly develop into adults, and (2) by determining the chronological order that R. pomonella races and sibling species break diapause and eclose when reared under standardized environmental conditions. The results imply that factors affecting initial diapause depth (and/or differential mortality during the prewintering period) and those determining the timing of diapause termination or rates of post-diapause development are both under differential selection and are to some degree genetically uncoupled in flies. The modular nature of diapause life history adaptation in Rhagoletis suggests that phenology may involve multiple genetic changes and represent a stronger ecological barrier separating phytophagous specialists than is generally appreciated.

Hormonal mechanisms underlying termination of larval diapause by juvenile hormone in the bamboo borer, Omphisa fuscidentalis

Topical application of methoprene, a juvenile hormone analogue (JHA), induces pupation by activating the prothoracic glands (PGs) in diapausing larvae of the bamboo borer, Omphisa fuscidentalis. To determine the minimum stimulation period for PG activation, we transplanted PGs of JHA-treated larvae (donors) into non-treated larvae (recipients) on successive days after JHA treatment and observed the recipients for pupation. JHA stimulation for 1 day was sufficient to induce pupation. In recipient larvae, the hemolymph ecdysteroid titer increased transiently on day 18 after transplantation and significantly on days 24–28, prior to pupation. Secretory activity of recipient PGs increased transiently on day 16 and days 22–28. Because the recipient PG activity was too low to account for an increased ecdysteroid titer, the JHA-stimulated donor PGs must produce the major part of hemolymph ecdysteroids. In addition, the ecdysteroid produced by the donor PGs might have stimulated the recipient PGs. We examined the possible involvement of two ecdysone receptor ( EcR) isoforms, OfEcR-A and OfEcR-B1, in PG activation by JHA, and found that although both isoforms were up-regulated, accompanied by an increased ecdysteroid titer in the hemolymph, the isoform mRNA levels were not altered at all before the increase in PG secretory activity. Thus, EcR expression might not be involved in feedback activation of PGs.

Resting stage density and hatching of two cladoceran species from small ephemeral waters

We investigated resting stage densities of two cladocerans, Daphnia obtusa and Moina macrocopa, in very small and ephemeral water bodies (temperate zone rain puddles) and tested whether these species exhibit a prolonged diapause in such an environment. Densities of ephippia as well as resting eggs in puddles ranged between 10 2 and 10 4 per m 2 , and varied substantially within as well as among puddles. We determined the hatching success and temporal dynamics for resting stages collected from natural habitats and incubated at 15 °C with a 14L:10D light regime. Hatching success of both species was high (> 80 %) and steady, with new hatchlings appearing mostly within 3-8 days. M. macrocopa hatched significantly faster and slightly more successfully than D. obtusa. Decapsulation of D. obtusa ephippia had no effect on the hatching success but slowed down the hatching dynamics. Hatching of egg pairs from the same ephippium was mostly synchronised - in only less than 10 % of cases one egg hatched and the other remained potentially viable for the next flooding event. We compare our results with available data on cladoceran resting egg densities and hatching success, and discuss the possible causes of the high and steady hatching proportion of puddle cladocerans. A physiologically-based bet-hedging strategy may not be necessary if only a certain proportion of eggs are exposed to hatching cues or when the hydroperiod of temporary waters is longer than the cladoceran life cycle. Additionally, frequent destruction of localities may promote instantaneous termination of diapause even in ephemeral habitats such as puddles.

Dynamism in physiology and gene transcription during reproductive diapause in a heteropteran bug, Pyrrhocoris apterus

Reproductive diapause was characterized in females of Pyrrhocoris apterus using physiological parameters (diapause intensity, photoperiodic responsiveness, oxygen consumption, mass and hydration) and changes in relative abundance of mRNA transcripts of eight different genes coding for proteins implemented in energy metabolism, cryoprotectant biosynthesis, biological clocks, and hormonal receptors. Changes in diapause intensity served as a basis for distinguishing successive phases of diapause development, which were driven both endogenously (under constant environmental conditions) and exogenously (in response to a change in environmental conditions). Changes in the relative levels of transcripts of genes coding for aldose reductase ( AR) and sorbitol dehydrogenase ( SoDH) closely matched those of diapause intensity and thus appeared as promising molecular markers of diapause and its development. During the initiation phase, the intensity of diapause and the levels of AR and SoDH transcripts increased and reached a maximum. During maintenance, under a constant temperature of 20 °C and short-day photoperiod, the intensity of diapause and the levels of both transcripts first decreased and, later, were maintained constant. Termination of diapause was stimulated by cold, during which the intensity of diapause and the levels of both transcripts further decreased. Upon resumption of direct development (oogenesis, mating and oviposition), the relative abundances of AR and SoDH transcripts decreased to trace levels.

Effects of nutrition and methoprene treatment upon reproductive diapause in Caloptilia fraxinella (Lepidoptera: Gracillariidae)

Abstract Female Caloptilia fraxinella exhibit a prolonged reproductive diapause immediately post adult emergence in mid‐summer until the next spring when mating, egg development and oviposition on fresh Fraxinus spp. leaflets occur. Factors that effect the termination of reproductive diapause are investigated in this species. Caloptilia fraxinella diapausing adults held in overwintering conditions (2 °C, LD 0 : 24 h) for 24 weeks terminate diapause after placement for 2 weeks in simulated summer conditions (24 °C, LD 16 : 8 h) only if they are provided with 10% sugar water. Exogenous application of the Juvenile Hormone (JH) analogue methoprene to moths in both early‐ (summer) and mid‐ (autumn) reproductive diapause demonstrates that JH affects diapause termination but a carbohydrate nutrition source also mediates mating and vitellogenesis. Mating between moth pairs early in diapause occurs only after treatment with methoprene and provision with sugar water. However, there is no impact of mating on the propensity of females to produce vitellogenic oöcytes. Moths collected in the autumn in mid‐diapause respond in a dose‐dependent fashion to methoprene treatment and the response is greater than that of moths early in diapause collected in the summer. Treatment with methoprene and access to sugar water results in vitellogenic oöcytes in 18.75% of females from mid‐diapause moth pairs treated with 0.01 μg methoprene per insect and in all females from pairs treated at the two highest doses of methoprene (0.1 and 1 μg per insect). Mating occurs only between moths in mid‐diapause treated with the two highest doses of methoprene and these doses induce 91% and 100% mating, respectively. Both control and methoprene‐treated males in mid‐diapause held under summer conditions mate successfully and pass a spermatophore to their methoprene‐treated female partner. These data demonstrate that female C. fraxinella undergo a prolonged reproductive diapause in which termination is dependent on JH and further mediated by a carbohydrate nutrition source. The production of vitellogenic oöcytes is independent of mating. These data also provide evidence that response of moths in diapause to exogenous applications of methoprene differs throughout the diapause period and between male and female C. fraxinella.

20.P1. Effects of temperature and light on embryonic diapause termination in Artemia dormant cysts that have never been desiccated

20.P1. Effects of temperature and light on embryonic diapause termination in Artemia dormant cysts that have never been desiccated

20.5. A comprehensive study of Artemia genes activated in a cold treatment to induce embryonic diapause termination

20.5. A comprehensive study of Artemia genes activated in a cold treatment to induce embryonic diapause termination

High temperature and hexane break pupal diapause in the flesh fly, Sarcophaga crassipalpis, by activating ERK/MAPK

Pupal diapause in the flesh fly, Sarcophaga crassipalpis, can be terminated by exposure to high temperatures or, artificially, with a topical application of organic solvents. To analyze the molecular mechanisms involved in diapause termination we explored the possibility that the mitogen-activated protein kinases (MAPK) are involved in this response. Levels of phospho-ERK increased within 10 min after hexane application. Extracellular signal-regulated kinase (ERK) was also activated when pupae were transferred from 20 to 25 °C, thus suggesting that ERK activation is a likely component of the signal transduction pathway used to initiate development in response to diapause-terminating signals. 20-Hydroxyecdysone and cyclic GMP terminate diapause in this fly, and the juvenile hormone analog methoprene shortens the diapause, but none of these agents activated ERK. ERK was readily activated in isolated abdomens treated with hexane, thus we conclude that ERK is directly activated by the hexane treatment. ERK activation was evident in the brain, epidermis, midgut and fat body, but not in the ventral nerve mass or ring gland, thus suggesting that ERK does not act directly on the ring gland to promote ecdysteroid synthesis but exerts its effect through stimulation of the brain.

Life History Traits of &lt;I&gt;Pseudasphondylia rokuharensis&lt;/I&gt; (Diptera: Cecidomyiidae) Affecting Emergence of Adults and Synchronization with Host Plant Phenology

To identify adaptive strategies of gall-inducing cecidomyiids, we studied the life history traits of Pseudasphondylia rokuharensis (Diptera: Cecidomyiidae), a univoltine species inducing fruit galls on a deciduous shrub, Viburnum dilatatum. Although univoltine gall midges that are associated with trees or shrubs are usually difficult to rear from immature stages under artificial conditions, we successfully reared P. rokuharensis from first instar to adult. Mature larvae entered diapause in autumn, and the diapause terminated after low temperature treatment (4 mo of incubation at 5 degrees C). The adults emerged within a shorter period of time than those without low temperature treatment. Thus, the diapause provides better synchronization of adult emergence in the spring. Because adults live for only a few days, this synchronization improves the chances of adults finding a mate. This is the first report on the mechanism of larval diapause termination for univoltine and tree- or shrub-associated gall midges. The numbers of days needed for adults to emerge under laboratory conditions after low temperature incubation were significantly different between two different localities. This result might suggest the possible existence of ecoclines in their life history parameters.

Effect of the Juvenile Hormone Analog, Fenoxycarb on Termination of Reproductive Diapause in Scotinophara lurida (Burmeister) (Heteroptera: Pentatomidae)

This study was carried out to investigate a role of the juvenile hormone analog, fenoxycarb (FC) in terminating the reproductive diapause in the black rice bug, Scotinophara lurida (Burmeister) (Heteroptera: Pentatomidae). FC-treated adults collected at different dates developed their ovaries sooner than untreated ones. Topical application of FC accelerated diapause termination of field-collected S. lurida in which FC-treated adults exhibited early oviposition. In FC-treated males, development of their accessory glands and testes accelerated appeared to be prompted. These results suggest that various physiological overwintering traits related to diapause in this species may in part be under gonadotrophic endocrine control.

Correlation of oxygen consumption, cytochrome c oxidase, and cytochrome c oxidase subunit I gene expression in the termination of larval diapause in the bamboo borer, Omphisa fuscidentalis

The moth Omphisa fuscidentalis (Lepidoptera, Pyralidae) is a univoltine insect with a larval diapause period lasting up to 9 months. We studied changes in O 2 consumption in conjunction with cytochrome c oxidase activity and cytochrome c oxidase subunit I ( cox1) gene expression. O 2 consumption changed within a day, showing a supradian rhythm with a ca.12-h cycle at 25 °C. During the first two-thirds of the diapause period, from October to March, O 2 consumption was constant until January and then increased by March. Topical application of methoprene, a juvenile hormone analog (JHA), to diapausing larvae terminated the diapause and was associated with an increase in O 2 consumption rate at diapause termination. In JHA-treated larvae, cytochrome c oxidase activity in fat bodies was high at the beginning of the prepupal period and highest at pupation. cox1 expression in fat bodies displayed a transient peak 8 days after JHA application and peaked in the prepupal period. Taken together, our results show that the break of diapause by JHA is associated with the activation of cox1, bringing about an increase in cytochrome c oxidase activity, followed by an increase in O 2 consumption rate.