Winter Diapause Research Articles

First evidence of pupal summer diapause in Pieris brassicae L.: the evolution of local adaptedness

Pieris brassicae L. is adapted to a wide variety of local climates throughout the Palaeartic by means of geographic variation in daylengths and temperatures triggering winter diapause. We report for the first time a population from Sotogrande in southern Spain (strain S) that additionally exhibits a pronounced summer diapause in the pupal stage as a response to long daylengths. As well as having diapause triggered by long daylengths, this population develops directly at short, ecologically relevant daylengths. This unusual short-day type response is expressed at temperatures of 21°C and above. The absence of cryptic summer diapause in a population from southern France indicates that this summer diapause evolved locally in Spain or Northern Africa in a population of P. brassicae which lacked this trait. The PPRs of strains S, H (Denmark) and B (France) and crosses between them suggest that summer diapause is inherited as a recessive allele which has a clinal decrease of frequency in populations northwards. The population from southern France shows that this simple pattern of inheritance is further modified by an unknown genetic mechanism controlling the expression of summer diapause near the border between aestivating and non-aestivating populations. On the basis of the photoperiodic response and climatic data we predict P. brassicae to have five or more generations each year in southern Spain.

Diapause and survival in winter in two species of predatory bugs, Orius sauteri and O. minutus

AbstractThe cause of differences in overwintering success between the sexes in Orius sauteri (Poppius) and O. minutus (Linnaeus) (Heteroptera: Anthocoridae) was investigated in the laboratory. The survival rate of adults was examined in a screen house outdoors during the winters of 1995–1996 and 1996–1997. None of the males of either species survived until spring in either year. However, 63.9% and 40.5% of the females in O. sauteri and O. minutus, respectively, survived the winter in 1995–1996, and 54.5% and 43.2%, respectively, in 1996–1997. Most of the males died by early winter. In both species, the adult females reared under short days (= L11:D13) survived for a long period at 5 or 0 °C, while the males reared under the same photoperiod died shortly after transfer to 5 or 0 °C from 22 °C. The males and females kept at same temperature conditions under long days (= L16:D8) died early. When nymphs were kept under long days at 22 °C, the lipid content in the female and male adults of O. sauteri was 27.9% and 17.7%, respectively. When nymphs were kept under short days, their lipid content was significantly higher (41.1%) than that of those reared under long days for females, but lipid content was comparable in the males regardless of photoperiod (15.6%). In O. minutus, the mean lipid content was 27.2% in females and 19.0% in males under long days at 22 °C, and 40.8% in females and 19.8% in males under short days. Thus, a large amount of lipid was accumulated only in females kept under short days in both species. These results suggest that short days induced diapause only in adult females but not in males. Due to the lack of diapause and shortage of lipid accumulation, males may not be able to survive the winter.

Long-term reduction of cold hardiness following ingestion of ice-nucleating bacteria in the Colorado potato beetle, Leptinotarsa decemlineata

We investigated the effect of ingestion of ice-nucleating bacteria on the supercooling capacity and cold hardiness of the Colorado potato beetle ( Leptinotarsa decemlineata Say), a freeze-intolerant species that overwinters as adults in shallow, terrestrial burrows. Ingestion of ice-nucleating bacteria ( Enterobacter agglomerans, Pseudomonas fluorescens, Pseudomonas putida, Pseudomonas syringae), fed on slices of potato tuber, caused an abrupt decrease in supercooling capacity. No change occurred in the supercooling capacity of beetles fed Escherichia coli, as this species lacks ice-nucleating activity. Ingestion rates showed that tubers treated with different species were equally palatable. During diapause induction beetles evacuated food from their guts, but nevertheless retained sufficient ice-nucleating bacteria to diminish supercooling. Beetles fed P. fluorescens and P. putida exhibited reduced supercooling even after an 8-wk exposure to simulated winter conditions. Furthermore, P. fluorescens was isolated 10-wk post-ingestion from diapausing beetles. Our data suggest that ingested bacteria may be retained by insects during entry into diapause and that the cold hardiness of candidate crop pests, such as L. decemlineata, may be reduced by feeding them ice-nucleating bacteria prior to winter diapause.

Life cycle strategies of epipelagic copepods in the Southern Ocean

Twelve epipelagic copepod species were reviewed to compare their adaptations to the short primary production season and low temperatures which characterise the Southern Ocean. The species show a spectrum of adaptations, but three broad life cycle strategies were defined: (1) herbivorous in summer, a short reproductive period and winter diapause at depth ( Calanoides acutus and possibly Ctenocalanus citer); (2) predominantly omnivorous/detritivorous diet, an extended period of feeding, growth and reproduction and less reliance on diapause at depth ( Metridia gerlachei, Calanus propinquus, Calanus simillimus, Oithona similis, Microcalanus pygmaeus, and possibly Oncaea curvata and Oithona frigida); (3) overwintering and feeding within sea ice as early nauplii or copepodids ( Stephos longipes and Paralabidocera antarctica). The large species Rhincalanus gigas appears to be intermediate between strategies (1) and (2). Contrasting species from groups (1) and (2), namely C. acutus and O. similis, were selected for more detailed comparison. For C. acutus, maximum (probably food saturated) feeding and egg production rates are well below equivalent values for Calanus spp. at lower latitudes. Likewise, summer growth and moulting rates are slower, and the growth season of this herbivore is only 2–4 months. Therefore, both the low summer temperatures and short primary production season seem to dictate a long (∼1 year) life cycle for C. acutus. A collation of data on O. similis revealed that its abundance increases about tenfold from the Antarctic shelf northwards to the Polar Frontal Zone, where abundances are similar to those in temperate and tropical shelf seas. In contrast to C. acutus, O. similis appears to remain in the epipelagic and reproduce there year-round, although the food sources which sustain this are still uncertain.

Daylength and Temperature Control of Predation, Body Size, and Rate of Increase in Toxorhynchites rutilus (Diptera: Culicidae)

Subtropical Toxorhynchites rutilus (Coquillett) frequently overwinter as 4th instars in treeholes of peninsular Florida. Exposure from hatch to short daylengths induced 4th instar diapause in over 50% of wild T. rutilus from southern Florida. Short daylengths and lower temperatures significantly reduced prey consumption rates. At a low frequency, diapausing larvae killed prey without consuming, which behavior increased with time in the 4th instar and was distinct from killing by prepupae. Termination of diapause by transfer of 4th instars to long daylengths was accompanied by an increase in prey consumption rate prior to pupation. Mean pupal masses were significantly affected by photoperiod and temperature treatments, confirming a correlation between heavier pupae and colder temperatures in the field. At 25°C and 21°C, female pupae were significantly larger than males, in contrast to no sexual size difference observed for continuous development at 27°C. The composite index of performance (r’), an analog of the per capita rate of increase, for diapausing cohorts was one-half to two-thirds of that estimated for non-diapausing cohorts, but temperature alone did not affect r’ between 25 and 21°C. Low rates of prey consumption during winter diapause may contribute to the relatively modest, albeit significant, effect of T. rutilus predation on mosquito abundance as estimated from long-term censuses of treeholes.

Control of summer and winter diapause in Pidorus euchromioides (Lepidoptera: Zygaenidae) on Chinese sweetleaf Symplocos chinensis

AbstractPidorus euchromioides Walker has two separate diapauses during its life cycle, a winter diapause as a fourth larval instar and a summer diapause as a prepupa in a cocoon. Winter diapause was induced by short photoperiods. The critical day length of 13 h 20 min to 13 h 40 min at 23.3°C under insectary conditions was very similar to the critical day length (13 h 32 min) observed in the field. Sensitivity to day length was restricted to the first 9 days, corresponding to the first and second instars. The duration of larval diapause was not only strongly correlated with the inducing photoperiod, but also dependent on the number of short days experienced during the larval growth period. The shortest diapause occurred at the critical day length, or when the larvae were exposed for 6 days (a critical number of short days) to a photoperiod of LD 12 h:12 h. The summer diapause appeared to be primarily determined by a genetic factor and only occurred in part of the overwintering generation and the first generation. The two different diapause mechanisms play important roles. Winter diapause ensures that P. euchromioides synchronizes its development and activity with the phenology of specific host plants, and summer diapause provides the species with a high degree of adaptation to an unpredictable environment.

Altitudinal differentiation in the diapause response of two species of dung flies

1. Seasonality is a prime selective factor promoting genetic differentiation of populations. Local adaptation in diapause response was investigated in the two geographically and altitudinally widespread dung flies Scathophaga stercoraria (Diptera: Scathophagidae) and Sepsis cynipsea (Diptera: Sepsidae).2. Replicate sibships from three sites in Switzerland with low and high altitude dung fly populations were raised in a common laboratory environment simulating the natural decreasing photoperiod and temperature regimen before winter. From field phenologies, the critical photoperiod inducing diapause was predicted to be longer for high than for low altitude populations (12 vs. 10 h for Sc. stercoraria, and 12.25 vs. 11 h for Se. cynipsea) if they are locally adapted.3. Contrary to expectation and to Sc. stercoraria, which diapauses in the pupal stage, Se. cynipsea diapauses in the adult stage.4. Low but significant levels of genetic differentiation in pre‐winter adult emergence were evident between low and high altitude populations of both species, but they were far from the differences predicted. Scathophaga stercoraria also showed geographical differentiation independent of altitude.5. Sepsis cynipsea females stopped reproducing at some point before winter, but altitude did not affect the timing of adult diapause. High altitude females and females that did not initiate reproduction before winter survived the simulated winter better.6. Both species largely used temperature rather than photoperiod as a cue inducing winter diapause, an untypical case of phenotypic plasticity. The hypothesis that Sc. stercoraria, whose generation times are much longer than those of Se. cynipsea, responds to a greater extent to temperature rather than photoperiod only was rejected.

Genetic basis of photoperiodic control of summer and winter diapause in geographic ecotypes of the rice stem maggot, Chlorops oryzae

Abstract Chlorops oryzae Matsumura (Diptera: Chloropidae) is bivoltine in northern Japan but trivoltine in the southern part of the country. Larvae of the bivoltine strain (Akita, 39° N) develop without delay under L14:D10 but enter summer diapause in the mature larval stage under L15:D9. In contrast, larvae of the trivoltine strain (Aichi, 35° N) develop quickly under L15:D9 but enter summer diapause under L14:D10. The genetic basis of their different summer‐diapause behavior was analyzed by reciprocal crossing between the two ecotypes and backcrossing to the hybrids. Although a polygenic system seems to be involved, there is a single gene on the X‐chromosome exerting a major effect on summer diapause. The northern bivoltine ecotype has a longer critical photoperiod for the induction of winter diapause in the first larval stage and remains in diapause longer than the southern trivoltine ecotype. The differences in the critical photoperiod and the winter diapause duration between the two ecotypes seem to be controlled by a polygenic system but again a sex‐linked or closely linked gene (or genes) plays a major role. The two geographic ecotypes differ significantly in summer‐ and winter‐diapause traits, both of which are characterized by sex‐linked inheritance. Despite this, no apparent sterility or inviability in hybrids between the ecotypes occurs.

Effects of temperature and winter diapause on survival and development in bivoltine and trivoltine ecotypes of the rice stem maggot, Chlorops oryzae Matsumura (Diptera : Chloropidae), reared on a winter host

In Chlorops oryzae, winter diapause in the first larval stage is induced by short days in the egg stage and maintained by short days in the larval stage. On wheat plants (winter host), most diapause and non-diapause larvae failed to pupate and died within 50 days at 23°C regardless of photoperiod. When diapause larvae were reared on wheat plants at 10, 15 or 20°C under LD12 : 12, the survival rates increased with decreasing temperatures. Diapause development at 10°C was completed about 70-90 and 40-50 days in the Akita (bivoltine, 39°N) and Aichi (trivoltine, 35°N) strains, respectively. The survival rates on wheat seedlings at 23°C in diapausing larvae of the Akita strain increased with increasing periods of previous exposure to 10°C from 41 to 80 days. Aichi larvae showed higher survival rates regardless of the period at 10°C. It appears that low temperature promotes survival of the larvae on wheat plants, and larvae which complete diapause development can grow to the pupal stage on winter hosts.

Effect of juvenile hormone analogs on diapause termination and myo-inositol content in Aulacophora nigripennis adults (Coleoptera : Chrysomelidae)

Aulacophora nigripennis adults have winter diapause and accumulate myo-inositol during winter. To elucidate the relationship between diapause state and myo-inositol metabolism, two kinds of juvenile hormone analog (JHA), methoprene and pyriproxyfen, were topically applied to the diapausing beetles and subsequent changes in diapause state and myo-inositol content were observed. Application of JHA terminated diapause and also inhibited myo-inositol accumulation. These observations suggest that diapause state and myo-inositol content of this beetle are regulated by the JH endocrine system, although it remains unsolved whether the disappearance of myo-inositol was caused by direct action of JH or by an indirect effect accompanied by diapause termination.

Life cycles of two limnetic cyclopoid copepods, Cyclops vicinus and Thermocyclops crassus, in two different habitats

The life cycles of Cyclops vicinus and Thermocyclops crassus in two shallow eutrophic habitats, Junsainuma and Naganuma Ponds, Hokkaido, Japan, were investigated. Both ponds exhibited similar seasonal patterns of temperature, oxygen levels and pH during ice-free periods; however, oxygen levels were extremely lower under the ice in Naganuma Pond. Cyclops vicinus showed different life cycles in the two ponds; in Junsainuma Pond, it reproduced in winter and spring (January-May) and entered diapause during summer and autumn (June-October) as copepodite IV stage, while it reproduced in autumn (October-November) and spring (April-May), and entered diapause in summer (June-September) and winter (January and February) as copepodite V stage in Naganuma Pond. Thermocyclops crassus entered diapause during winter (December-April) as cope- podite IV and V stages in both ponds, and egg-bearing females appeared only during the warm season, from early May to late October, when water temperatures were >10°C. Summer diapause in C.vicinus was suggested to be an adaptation against fish predation, whereas C.vicinus entered winter diapause in Naganuma Pond probably to avoid low oxygen levels. Thermocyclops crassus entered diapause in both ponds to avoid low water temperature. These results suggest that biotic and abiotic factors are important for leading to specific life cycles of cyclopoid copepods in small water bodies. -

Summer and winter diapause in pupae of the cabbage butterfly, Pieris melete Ménétriés

The cabbage butterfly, Pieris melete is multivoltine with a pupal summer and winter diapause. Summer and winter diapause are induced principally by relatively long and short daylengths, respectively. The intermediate to relatively short daylengths of autumn permitted some pupae to develop without diapause in the field. A short daylength had a stronger diapause inducing effect than a relatively long one under higher temperatures. The principal sensitive phase for photoperiodic response occurred before the late 3rd larval instar. The critical daylength for wild autumnal populations was between 12 h 30 min and 12 h 40 min at an average temperature of 20.5°C. A night interruption by 2 h of light averted diapause most effectively when it was placed 10 to 12 h after lights-off. High temperatures and long days during summer inhibited the incidence of diapause, suggesting that the occurrence of summer diapause is due to the specific climatic conditions occurring in April and early May, rather than to the high temperatures in summer. This indicates that the butterfly has a cryptic ability to reproduce in summer. High temperatures delayed diapause development, whereas low temperatures enhanced it, indicating that the optimum temperature of diapause development is lower. The diapause regulating mechanisms thus ensure that the species synchronises its development and reproduction with the growth seasons of the host plants and provide the species with a high degree of flexibility in its life cycle.

Effects of temperature on growth, development and diapause in the yellow dung fly - against all the rules?

The effects of rearing temperature (and photoperiod) on growth, development, body size, and diapause induction and termination in the yellow dung fly, Scathophaga stercoraria, were investigated by allowing replicate families of larvae to develop in the field along a time sequence approaching the onset of winter. This was supplemented with extensive laboratory rearing. At constant laboratory temperatures, growth rates were maximal between 15°C and 20°C and decreased at higher (25°C) and lower (10°C) temperatures, while the development rate was maximal at 25°C. Perhaps related to this, yellow dung flies reached a given size faster at naturally variable, as opposed to constant, temperatures. In the field, lower temperatures towards the end of the season resulted in larger individuals that grew faster. Adult body size increased as development time, expressed in calendar days, increased, a positive relationship commonly taken for granted in life history theory, but decreased as development time expressed in degree-days increased. The effect of temperature on growth, development and body size can thus change or even reverse if individuals can alter their growth rate independently of development time, and if the physiological effects of temperature are factored out by converting development time into degree-days above a lower development threshold. Therefore, supposedly well-established trends possibly need to be re-examined along these lines. Pupal winter diapause towards the end of the season was highly reversible by temperature. Pre- and post-winter emergence patterns together suggest that the minimum time for yellow dung flies to successfully complete development, at any time of the year, is about 230-250 degree-days.

Effect of temperature and photoperiod on diapause development in a Douglas fir seed chalcid, Megastigmus spermotrophus.

Douglas fir seeds infested by diapausing larvae of a chalcid, Megastigmus spermotrophus, were transferred under different temperature and photoperiod regimes at various dates during autumn and winter. Both winter diapause and prolonged diapause were compared to the diapause patterns observed in control lots kept under natural conditions. The results showed that exposure to low temperatures in autumn and winter is required for the completion of diapause development. Median adult emergence dates and the date of transfer of larvae to 20°C were negatively correlated. The frequency of prolonged diapause of larvae transferred to 20°C decreased significantly after November. When larvae were submitted to different constant temperatures, the longer the daylength, the higher and faster the reactivation. These results suggest that chalcid larvae can perceive daylength through the seed coat. This phenomenon is probably related to the fact that most of the infested seeds falling in autumn are usually covered by a layer of leaf litter during the winter.

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.

Degree-Day Accumulations and Seasonal Duration of the Pre-Imaginal Stages of the Mexican Fruit Fly (Diptera: Tephritidae)

Degree-day accumulations and puparial duration of the Mexican fruit fly, Anastrepha ludens (Loew), in the field was found to fit closely with a degree-day accumulation model developed by Leyva-Vazquez (1988) with laboratory data. Larval development time was more variable, however, and did not agree well with the laboratory based degree-day model. This may have been caused by a tendency of the larvae to remain in the fruit beyond the necessary development time and for subsequent egression to be spread over a period of weeks. Duration of the pre-imaginal stages is strongly a function of season. The puparial stage may be prolonged up to three months in the winter or be as brief as three weeks in the summer. There was no evidence of a winter diapause.

Stage-Dependent Changes of the Prothoracicotropic Hormone (PTTH) Activity of Brain Extracts and of the PTTH Sensitivity of the Prothoracic Glands in the Cabbage Armyworm, Mamestra brassicae, before and during Winter and Aestival Pupal Diapause

The cabbage armyworm, Mamestra brassicae, enters winter and aestival diapause in the pupal stage under 10L-14D and 16L-8D, respectively, at 23°C. It develops without pupal dormancy under 14L-10D at 23°C. In 6th-instar larvae, the hemolymph ecdysteroid titers as well as the activity and sensitivity of the prothoracic glands (PGs) were nearly the same in the diapause- and nondiapause-programmed larvae. In non-diapause pupae (ND-pupae), the ecdysteroid titer peaked in the first half of the pupal stage. By contrast, in winter and aestival diapause pupae (WD- and AD-pupae), the ecdysteroid titer remained low after pupation. The ecdysteroid titer in diapausing AD-pupae was 8- to 10-times higher than that in diapausing WD-pupae. PGs from 5th-instar and 6th-instar larvae, as well as those from pupae, secreted ecdysteroids and showed a far stronger response to big prothoracicotropic hormone (PTTH) than to small PTTH in vitro. PG activity and its sensitivity to big PTTH fluctuated in a stage-dependent manner, and the pattern was nearly the same for 6th-instar larvae committed to develop into ND-, WD- or AD-pupae. When ecdysteroids for larval-pupal metamorphosis appears in the hemolymph of 6th-instar larvae, the activity and sensitivity of the PGs may be suppressed quickly. After pupation, the titer of hemolymph ecdysteroids as well as the activity and sensitivity of the PGs may be related to the strength (or duration) of pupal dormancy which differs between WD-pupae and AD-pupae.

Induction and Termination of Winter Diapause in a Californian Strain of the Cabbage Maggot (Diptera: Anthomyiidae)

Populations of the cabbage maggot, Delia radicum (L.), occur in the field during all seasons in coastal northern California because the climate is mild, hosts are available, and a percentage of the population does not enter diapause. Laboratory experiments on this population of the cabbage maggot showed the following 6 results: (1) criteria for diapause vary with the conditions that induce diapause, (2) the proportion of larvae entering diapause is highest at low temperatures across all photoperiods and at short photoperiods across all temperatures, (3) developmental times of larvae producing diapause pupae were longer than for those producing nondiapause pupae, (4) rearing larvae at high temperatures and short photoperiods increased the diapause period for the pupal stage, (5) average pupal weights of diapause pupae (20.20 ± 2.27 mg) (mean ± SD) were higher than for nondiapause pupae (18.01 ± 3.31), and (6) fresh pupae weighing <15.5 mg did not complete diapause. The results support previous findings that field populations of D. radicum are induced into winter diapause mainly by short photoperiods, whereas temperature has a lesser effect.

Feeding and digestive activity of cyclopoid copepods in active diapause

Three different methods were used to compare the feeding patterns of active cyclopoids and cyclopoids in active diapause from different habitats. First, we offered 14C- labeled algal detritus to stage III, stage IV (two different physiological groups), and adult females of Acanthocyclops vernalis from temporary water-bodies of the Volga Delta. Second, we compared the functional responses of active and actively diapausing cyclopoids preying on copepod nauplii. Stage III, stage IV (various physiological groups), stage V, adult males and females of Acanthocyclops viridis, Cyclops kolensis, C. abyssorum sevani from the Volga Delta, Lake Sevan (Armenia), and Mozhaisk Reservoir (Moscow District) were tested. Finally, we examined the activity of digestive enzymes (proteases) of CIV of C. kolensis from Mozhaisk Reservoir at different temperatures and temperature acclimation regimes. All three approaches used have led to similar conclusions. Actively diapausing cyclopoids were capable of feeding on both plant and animal prey; however, their feeding rates and digestive enzyme activity were 2–8 times lower than those of active cyclopoids of similar size. At the initial stage of active diapause the feeding rates were comparable with those of active cyclopoids then declined to a low level during approximately two weeks. Transfer of cyclopoids undergoing winter diapause from ambient temperature (4 °C) to warmer water (20 °C) resulted in dramatic increase of proteases activity only if the acclimation period was relatively long (two weeks).

Photoperiodic Induction, Maintenance and Termination of Winter Diapause in Two Geographic Ecotypes of the Rice Stem Maggot, Chlorops oryzae MATSUMURA (Diptera: Chloropidae)

The sensitivity of Chlorops oryzae MATSUMURA to photoperiod in controlling winter diapause was studied by changing photoperiod at various stages. A short day (12 h) in the egg stage induced a winter diapause in the first larval stadium. The latter half of the egg stage was most sensitive to the diapause inducing photoperiod. Short days in the larval stage maintained diapause, but long days terminated it. In the bivoltine strain (39○N), three short-day cycles were required to induce diapause when the egg stage lasted for 9 days. The critical photoperiod during the egg stage for the induction of diapause was about LD14:10. The duration of diapause under LD12:12 was 80 to 90 days. The critical photoperiod in the larval stage for the maintenance of diapause was about LD14:10. Winter diapause in the viboltine strain sampled in December was maintained under LD12:12, but short and long days had similar effects on development when insects were sampled in January. In the trivoltine strain (35○N), 4 short-day cycles were required to induce diapause when the egg stage was 9 days. The critical photoperiod for the induction and maintenance of diapause at 20°C was about LD13:11. The duration of diapause under LD12:12 was 50 to 60 days.