The embryonic diapause of Aulocara elliotti (Orthoptera,Acrididiae)

Progressive hypertrophy of fat body, muscles, gonads and pleuropodial glands was observed with lengthening diapause incubation in embryos of Aulocara elliotti. Embryonic hemolymph stained more darkly and lipoid materials accumulated in the fat body and other tissues. Gradual increase in volumes was observed in the corpora cardiaca, corpora allata and ventral head glands (ecdysial glands). Termination of diapause was achieved in embryos treated with juvenile hormone analogue (JHA) (4 ethyl phenyl 6.7 epoxy geranyl ether--87%, Stauffer Chemical) applied directly to the egg undiluted or when eggs were immersed in a 10% solution in methanol. Treated embryos terminating diapause underwent rapid teratological morphogenesis, achieving pigmentation and sclerotization as in definitive embryos without engulfing their yolk. In treated embryos which remained in diapause, unusual paired masses of pigmented cells, resembling the melanotic pseudotumors of Drosophila, were observed ventral and lateral to the stomodeum and are thought to be subesophageal body cells (pericardial cell homologues). In some embryos these cells were enlarged, lysed or their nuclei rhexic and pycnotic. This response suggests these cells are target organs for JHA, or perhaps for ecdysone or its precursor released by JHA treatment. Endocrine glands in treated embryos had significantly larger volumes (.01) than those of controls or untreated embryos. The ventral head glands of treated embryos appeared to be cytoplasmically depleted. It is suggested that JHA triggered the release of stored ecdysone (or its precursor produced in the ventral head gland) at a rate too rapid for normal morphogenetic processes, such as dorsal closure, to accompany epidermal maturation. The response to JHA cannot be interpreted as juvenilization, but rather must be considered to be precocious maturation. These results indicate that: 1. diapause development involves a transfer of nutrient materials from the yolk into the fat body and other embryonic tissues where they are available to meet the demands of post-diapause morphogenesis; 2. that embryonic diapause in A. elliotti is a consequence of endocrine deficiency which probably results ultimately from the lack of neurosecretory stimulus from the brain-corpora cardiaca complex; and 3. that the subesophageal body cells, and perhaps the pericardial cells, play an essential role in the embryonic physiology, perhaps in the production of carrier protein and/or an essential growth regulator.     

Inheritance of the photoperiodic response controlling imaginal summer diapause in the cabbage beetle, Colaphellus bowringi

Adults of the cabbage beetle Colaphellus bowringi display a summer diapause in response to the exposure of their larvae to long photoperiods. In the present study, the inheritance of the photoperiodic response controlling summer diapause in C. bowringi by crossing a high diapause strain (D strain) with a laboratory selected nondiapause strain (N strain) was investigated under different photoperiods at 22, 25 and 28 °C. The beetles in both reciprocal crosses and backcrosses showed a clear short-day response for the induction of diapause at all temperatures, similar to that of the D strain, suggesting that photoperiodic response of this beetle is heritable. The diapause incidences in the progeny from all the crosses under LD 15:9 or LD 12:12 at 25 °C suggest that genetic and genetic-environmental interactions are involved in diapause induction. The incidence of diapauses in F₁ progeny was significantly lower than that in the D × D strain but significantly higher than that in the N × N strain, indicating that the diapause capability is inherited in an incomplete dominant manner. The incidence of diapause was greater among the offspring of hybrid females when those females had a D strain mother or grandmother rather than a N strain mother or grandmother, indicating that maternal effects on diapause induction are stronger than paternal effects. The laboratory selected nondiapause strain also showed a short-day photoperiodic response at a low temperature of 22 °C, indicating that the photoperiodic photoreceptor and photoperiodic clock still function in the nondiapause strain.     

Diapause status of females affects attraction of male pear psylla, Cacopsylla pyricola, to volatiles from female-infested pear shoots

A companion study showed that male pear psylla, Cacopsylla pyricola (Förster) (Homoptera: Psyllidae) were attracted to volatiles from pear shoots infested with post-diapause females. The present study compared the behavioral response of males to diapause and post-diapause females. Assays were done using a Y-tube olfactometer. We collected male and female winterform psylla from pear orchards at regular intervals between late October (early diapause) and late February (post-diapause). Female-infested shoots were not attractive to males until the February samples, coinciding with ovarian maturation and onset of mating in the field. A second set of assays was done in which we manipulated diapause status in the laboratory either by exposing psylla to a long-day photoperiod or by treating insects with an insect growth regulator, fenoxycarb. In the photoperiod experiments, both short-day and long-day males preferentially selected long-day (post-diapause) females over short-day (diapause) females. Fenoxycarb-treated males preferred fenoxycarb-treated (post-diapause) females over untreated (diapause) females; untreated males showed no preferences. Results support observations made elsewhere that male winterform pear psylla perceive and are attracted to volatile odors associated with pear shoots infested with post-diapause females.     

Prevalence of kairomone-induced diapause in Daphnia magna from habitats with and without fish

The prevalence of the diapause response of the freshwater crustacean Daphnia magna to chemical cues on fish predation was evaluated in 35 clones originating from 14 European water bodies—inhabited or not inhabited by fish. Clonal lineages of experimental animals were cultured for 4 weeks in the presence or absence of water to which an extract of faeces of crucian carps (Carassius carassius), that were fed with Daphnia, was added. The proportion of females producing diapausing forms during the experimental period was used as a measure of the diapause response. A positive diapause response to fish predation cues was observed in 43% of investigated clones that originated from 71% of the water bodies tested. This indicated that the diapause response to fish scent is a common phenomenon in Daphnia magna from various locations in Europe. Surprisingly, no signs of a stronger diapause reaction to the tested cues were found in Daphnia originating from water bodies inhabited by fish compared with those from fish-free habitats.     

Biological characteristics of a non‐photoperiodic‐diapause strain of the cabbage beetle Colaphellus bowringi (Coleoptera: Chrysomelidae)

Comparison of biological characteristics between diapausing and non‐diapausing strains of insects provides some insights into the mechanisms regulating diapause. In this study, biological characteristics, especially diapause characteristics and life‐history traits, of a non‐photoperiodic‐diapause (NPD) strain of the cabbage beetle Colaphellus bowringi were compared with those of a normal, high‐diapause (HD) strain that enters diapause in response to either long day length or low temperature. The NPD strain did not enter diapause at any photoperiod at 22°C or higher, but still had a capacity to enter diapause at low temperatures. Although diapause could be induced in both strains by exposure to 20°C, the proportion of individuals having shorter diapause duration was greater in the NPD strain compared to the HD strain. The NPD strain had significantly lower hatching and larval survival rates, longer developmental duration of immature stages, smaller body size and lower longevity and female fecundity compared to the HD strain. The NPD strain of this species is a promising model for investigating diapause regulation in insects in general.     

Geographic variation in diapause induction: the grape berry moth (Lepidoptera: Tortricidae)

Diapause in insects occurs in response to environmental cues, such as changes in photoperiod, and it is a major adaptation by which insects synchronize their activity with biotic resources and environmental constraints. For multivoltine agricultural insect pests, diapause initiation is an important consideration in management decisions, particularly toward the end of the growing season. The grape berry moth, Paralobesia viteana (Clemens), is the main insect pest affecting viticulture, and this insect responds to postsummer solstice photoperiods to initiate diapause. Because the range of grape berry moth extends from southern Canada to the southern United States, different populations are exposed to different photoperiodic regimes. We quantified the diapause response in grape berry moth populations from Arkansas, Michigan, New York, Pennsylvania, Texas, and Virginia, and observed latitudinal variation in diapause initiation. Populations from Michigan, New York, and Pennsylvania responded significantly different than those from Arkansas, Texas, and Virginia. We also observed, as a consequence of our experiments, that the timing of our laboratory studies influenced grape berry moth's response to photoperiod, ceteris paribus. Experiments that were conducted when grape berry moth would be naturally in diapause resulted in a significant higher proportion of diapausing pupae at photoperiods (i.e., >15 h) that generally do not induce diapause, suggesting that attention should be paid to the timing of behavioral and physiological experiments on insects. This relationship between photoperiod and diapause induction in grape berry moth across geographic regions will provide applicable knowledge to improve pest management decisions.     

The prevalence of diapause response to risk of size-selective predation in small- and large-bodied prey species

The prevalence of diapause response to the simulated threat of fish predation was compared in three species of planktonic crustaceans of the genus Daphnia (D. magna, D. pulicaria and D. longispina), which due to their different body size vary in vulnerability to fish predation pressure in natural conditions. Higher incidence of diapause response was presumed in the larger-bodied species, which due to their higher conspicuousness and higher energetic content experience the greatest size-selective pressure from visually foraging fish. Small-bodied species were expected to utilize less costly yet less effective active defences, e.g. lower conspicuousness achieved due to slower body growth when facing risk of size-selective predation. Proportions of females forming diapausing structures as well as females body size at the maturation period were compared in experimental beakers containing or not containing fish kairomones (chemical cues of fish predation) in a few clonal lineages of 3 species of Daphnia derived from a single lake inhabited by fish. The highest incidence of diapause response to fish kairomones was observed in D. magna (when measured both as proportion of sensitive individuals and as proportion of inductive clones), the largest of the tested Daphnia species. The lowest proportion of individuals and clones that employed diapause was reported in the smallest tested species, D. longispina. In addition, the large-bodied Daphnia (D. magna) showed a greater reduction in body size in response to fish kairomones than the small-bodied species (D. longispina). The results of the present study support the assumption of higher prevalence of diapause response to the threat of selective predation in larger and more vulnerable prey species.     

Diapause strategy in the parasitoid Psyllaephagus pistaciae

The processes involved in the induction and termination of diapause in the parasitoid Psyllaephagus pistaciae Ferrière (Hymenoptera: Encyrtidae) were investigated under controlled laboratory conditions. Results indicated that the parasitoid P. pistaciae is able to overwinter successfully as a pupa within the mummified psyllid host Agonoscena pistaciae Burckhardt and Lauterer (Homoptera: Psylloidea), and the parasitoid clearly responded to a short photoperiod by entering diapause. The incidence of diapause increased significantly with decreasing temperature, indicating the existence of an interaction between low temperature and short‐day photoperiod that resulted in a 100% diapause. However, low temperature alone partly stimulated P. pistaciae to enter diapause. The incidence of diapause was likely to be independent from psyllid nymphal instar and the condition of its mother. This investigation showed that the termination of diapause in the overwintering parasitoid pupae and the duration of diapause completion or adult emergence is photoperiod independent, but dependent on temperature. However, chilling treatment was found to be unnecessary for diapause termination in P. pistaciae, although it decreased the duration of diapause maturation. The positive responses of parasitoids to environmental factors appears to act as a basic strategy to induce diapause in the parasitoid P. pistaciae against extreme climatic conditions.     

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.     

Effect of temperature on photoperiodic response in a selected 'non-diapause' strain of Pyrrhocoris apterus (Heteroptera)

Abstract. The artificially selected 'non-diapause' strain of Pyrrhocoris apterus (L.) (Heteroptera) showed no diapause response to photoperiod at 26°C (Socha & Hodkova, 1994). However, the diapause response to short-day photoperiod (LD 12:12 h) became apparent at lower temperatures of 17°C (70% diapause) or 20°C (41% diapause). Diapause was induced in 60% females by short-day photoperiod combined with thermoperiod of 26/16°C, whereas only 20% diapause was induced by the same thermoperiod under continuous darkness. Thus the time-measuring system was not removed by artificial selection but the diapause response was shifted to lower temperatures. The diapause response to short days seems to be favoured rather by low temperature during scotophase than by low temperature throughout the whole light/dark cycle. If the percentage of diapause at 26°C is compared in F₁ hybrids and in wild and selected parental strains the diapause appears to be dominant at LD 13:11 h but recessive at LD 11:13 h and LD 10:14 h. A hypothesis is proposed that the inheritance of the percentage of diapause in F1 hybrids is determined by interactions of genes controlling the temperature dependence of photoperiodic response.     

Diapause-specific gene expression in the northern house mosquito, Culex pipiens L., identified by suppressive subtractive hybridization

In this study we probe the molecular events underpinning diapause observed in overwintering females of Culex pipiens. Using suppressive subtractive hybridization (SSH) we have identified 40 genes that are either upregulated or downregulated during this seasonal period of dormancy. Northern blot hybridizations have confirmed the expression of 32 of our SSH clones, including six genes that are upregulated specifically in early diapause, 17 that are upregulated in late diapause, and two upregulated throughout diapause. In addition, two genes are diapause downregulated and five remain unchanged during diapause. These genes can be categorized into eight functional groups: genes with regulatory functions, metabolically-related genes, those involved in food utilization, stress response genes, cytoskeletal genes, ribosomal genes, transposable elements, and genes with unknown functions.     

Timing of diapause termination in relation to variation in winter climate

In temperate insects, winters are typically endured by entering diapause, which comprises a deep resting stage. Correct timing of diapause termination is vital for synchronization of emergence with conspecifics and for mobilizing resources when conditions for growth and reproduction become favourable. Although critical to survival, the intrinsic and extrinsic drivers of diapause termination timing are poorly understood. In the present study, we investigate diapause development under a range of durations (10–24 weeks) spent at different temperatures (?2 to 10 °C) in the pupal diapausing butterfly Pieris napi Linnaeus (Lepidoptera:Pieridae). We determine: (i) the maximum cold temperature for diapause development; (ii) if pupae in diapause count cold days or cold sums; and (iii) whether diapause termination is distinct or gradual. The results indicate large and idiosyncratic effects of high and low nonlethal temperatures on diapause development in P. napi. Although all temperatures tested lead to diapause termination, a thermal optimum between 2 and 4 °C is observed. Lower temperatures lead to decreased eclosion propensity, whereas higher temperatures slow down development and increase emergence desynchronization. These data suggest that, rather than a simple cold‐summing process with a distinct diapause termination point, there are trade‐offs between time and temperature at the low and high end of the thermal range, resulting in a nonlinear thermal landscape showing a ridge of increasing eclosion propensity at moderate temperatures. The present study suggests that the effects of temperature on diapause development should be included in projections on post‐winter phenology models of insects, including pest species.     

Differences in isolated mitochondria are insufficient to account for respiratory depression during diapause in artemia franciscana embryos

In response to cues signifying the approach of winter, adult Artemia franciscana produce encysted embryos that enter diapause. We show that respiration rates of diapause embryos collected from the field (Great Salt Lake, Utah) are reduced up to 92% compared with postdiapause embryos when measured under conditions of normoxia and full hydration. However, mitochondria isolated from diapause embryos exhibit rates of state 3 and state 4 respiration on pyruvate that are equivalent to those from postdiapause embryos with active metabolism; a reduction in these rates (15%-27%) is measured with succinate for two of three collection years. Respiratory control ratios for diapause mitochondria are comparable to or higher than those from postdiapause embryos. The P : O flux ratios are statistically identical. Our calculations suggest that respiration of intact, postdiapause embryos is operating close to the state 3 oxygen fluxes measured for isolated mitochondria. Cytochrome c oxidase (COX) activity is 53% lower in diapause mitochondria during one collection year; the minimal impact of this COX reduction on mitochondrial respiration appears to be due to the 31% excess COX capacity in A. franciscana mitochondria. Transmission electron micrographs of embryos reveal mitochondria that are well differentiated and structurally similar in both states. As inferred from the similar amounts of mitochondrial protein extractable, tissue contents of mitochondria in diapause and postdiapause embryos are equivalent. Thus, metabolic depression during diapause cannot be fully explained by altered properties of isolated mitochondria. Rather, mechanisms for active inhibition or substrate limitation of mitochondrial metabolism in vivo may be operative.     

Temperature and photoperiodic regulation of diapause of the southwestern corn borer,Diatraea grandiosella

The effect of temperature and photoperiod on the onset and termination of the mature larval diapause of the southwestern corn borer, Diatraea grandiosella, was examined. The results showed that diapause induction was an extremely temperature-dependent process. Larvae reared at 23°C under short days all entered diapause whereas 90 per cent of those reared at 27°C developed continuously. A photoperiodic response was only demonstrable at 25°C, when diapause was instituted following larval exposure to daily photophases ranging from 8 to 14 hr. An examination of the sensitivity of immature larvae to low temperatures revealed that all instars showed some susceptibility to low temperature induction of diapause. No intermediate instar was found in which the developmental programme could be switched entirely from a diapause to a non-diapause one, or vice versa.Diapause development was also found to be primarily temperature regulated. The rate of termination of diapause at 30°C was significantly higher than that at 25 or 23°C. Continuous exposure to light rather than a daily photoperiod produced the highest rate of diapause development. It was also shown that a period of chilling (5°C) did not accelerate diapause development. The significance of the results in relation to the evolution and geographical distribution of the species is discussed.     

Control of diapause and supercooling by the retrocerebral complex inPyrrhocoris apterus

Effects of external (photoperiod, temperature) and internal (retrocerebral complex, diapause condition) factors on supercooling were studied inPyrrhocoris apterus (L.) (Heteroptera: Pyrrhocoridae) adults. An increase in supercooling capacity is associated with the induction of diapause by short-day photoperiod or cardiacallatectomy of long-day non-diapause insects in spite of a high temperature of 26°C. The induction of diapause is a prerequisite for a further increase in supercooling capacity by cold acclimation. Post-diapause adults show low values of the supercooling point also in late January or early February, although their developmental potential is fully restored. Evidently the ability to supercool associated with diapause induction is maintained by a low ambient temperature in spite of diapause termination. The supercooling point increases rapidly when these adults are transferred to a high temperature of 26°C and cold re-acclimation is then no longer possible. The inhibition of morphogenesis (maturation of gonads) by cardiacallatectomy does not prevent the supercooling point from increasing in post-diapause adults at the high temperature.     

Inheritance of Diapause in Crosses between the Northernmost and the Southernmost Strains of the Asian Corn Borer Ostrinia furnacalis

The northernmost Harbin strain (N strain) of the Asian corn borer, Ostrinia furnacalis enters facultative diapause as fully grown larvae in response to short daylengths; whereas the southernmost Ledong strain (S strain) exhibits almost no diapause under the same light conditions. In the present study, we examined the inheritance of diapause induction and termination by crossing the two strains under a range of environmental conditions. The N strain showed a typical long-day response with a critical daylength of approximately15.88 h at 22°C, 15.72 h at 25°C and 15.14 h at 28°C, whereas the S strain showed a weak photoperiodic response at 22°C. The F1 progeny also showed a long-day response at 22, 25 and 28°C. However, the critical daylengths in S ♀ × N ♂ crosses were significantly longer than those in N ♀ × S ♂ crosses, indicating a sex linkage in the inheritance of diapause induction, with the male parent having more influence on the following F1 progeny. The incidence of diapause in S ♀ × N ♂ crosses was the same as in the N strain under short daylengths of 11-13 h, indicating that diapause trait is completely dominant over the non-diapause trait. The critical daylength in backcross to N was significantly longer than it was in backcross to S, showing a grandfather gene effect. Whether the inheritance of diapause fits an additive hypothesis or not was dependent on the rearing photoperiod, and the capacity for diapause was transmitted genetically in the manner of incomplete dominance. The duration of diapause for the reciprocal crosses under different diapause-terminating conditions showed different patterns of inheritance. The results in this study reveal that genetic and genetic-environmental interactions are involved in diapause induction and termination in O. furnacalis.     

Geographic variation in diapause response of adult Rhipicephalus appendiculatus ticks

Diapause in adults of the African brown ear tick Rhipicephalus appendiculatus is dependent on latitude and stock origin. Lower latitude populations, that is, those nearer the equator, show no diapause response to long or short day exposure. Diapause response to short day lengths is found in higher latitude populations, further south, and increases with increasing latitude. Nearly all individuals in the southernmost population, used in this study, enter diapause under short and long day exposure which implies that the onset of diapause in this population is obligatory. Diapause termination in higher latitude populations is induced by increasing photo period, further north, but still south of the equator, diapause is terminated by ageing. The differences in diapausing behaviour of the different populations are discussed in relation to their climatic conditions. This revised version was published online in July 2006 with corrections to the Cover Date.     

Role of temperature in diapause response to fish kairomones in crustacean Daphnia

The effect of non-lethal thermal conditions on the diapause response to a simulated threat of fish predation was tested in the freshwater planktonic crustacean Daphnia magna.From an early developmental stage, female Daphnia were either exposed or not exposed to fish kairomones that notified of the threat of fish predation at the benign growth temperatures of 18, 22 or 26 °C. The proportion of females switching from the production of subitaneous to diapausing eggs and their rate of reproduction were recorded.Besides the faster development and more intense reproduction observed at higher temperatures, a smaller proportion of the females formed protective, diapausing eggs when exposed to fish kairomones than was the case in colder conditions. The production of diapausing eggs was not observed when the threat of fish predation was absent. These results indicate an interactive effect of fish kairomones and thermal conditions on diapause induction in D. magna.We interpret these findings in the context of strategies for the maximisation of reproductive success. The production of well protected diapausing eggs (which assures low yet stable gains under diverse thermal conditions) may be a more beneficial life history strategy at lower temperatures, where the chances of survival of active individuals until maturation and successful reproduction are low. Higher temperatures permit faster maturation and more intensive reproduction that may surpass numerical losses of active descendants due to predation, making diapause a less rewarding option.     

Presence of three diapauses in a subtropical cockroach: control mechanisms and adaptive significance

Abstract.  Diapause is common among insects and is regarded as an adaptive response to periodic occurrence of adverse conditions. It occurs at a particular developmental stage, typically only once in a lifetime. However, little is known about the details of the control mechanism of life cycles with multiple diapauses in insects. In this study, a complex 2-year life cycle with three types of diapause is reported in a subtropical cockroach, Symploce japonica : a winter diapause in mid-nymphal instars, a summer diapause in later nymphal instars, and a reproductive diapause is reported in the adult stage. Nymphal development was extremely slow either at short days (winter diapause) or long days (summer diapause). Nymphs in summer diapause matured rapidly when transferred from long days to short days, indicating that seasonal changes in day-length are the pivotal factor in the control of this life cycle. It is proposed that the main significance of winter diapause in this subtropical species is to enable the nymphs to survive the mild winter successfully with reduced energy demand, and that of summer diapause is to delay adult emergence until late in the autumn for successful induction of the following adult diapause. Adults do not emerge until shortly before winter, yet the presence of diapause in the adult stage does not simply appear to be a response to cope with the winter conditions but, instead, ensures that reproduction will occur early the next year, before summer, because reproduction is greatly hampered at high temperature.