State Of Diapause Research Articles

Metabolic cold adaptation in arthropods: a smaller‐scale perspective

Metabolic cold adaptation in arthropods: a smaller‐scale perspective

Genetic diversity and widespread haplotypes in a migratory dragonfly, the common green darner Anax junius

Abstract. 1. Species that undertake regular two‐way migration may be expected, through population connectivity, to exhibit some level of genetic similarity over broad spatial scales. Although seldom following two‐way migration, highly mobile insect species tend to exhibit either low haplotype diversity and no phylogeographic structuring, or relatively high haplotype diversity and pronounced phylogeographic structuring.2. This study reveals the first wide‐scale genetic characterisation of a migratory dragonfly, the common green darner Anax junius Drury. Unusually for insects, north‐south two‐way migration is common in this species, although not obligatory. In at least part of its range, some individuals follow an extended developmental period and overwinter in a state of diapause.3. Mitochondrial sequence data were obtained from 92 A. junius individuals collected from 35 sites across Canada, U.S.A., and Mexico. These revealed 38 haplotypes, some of which were extremely widespread, although the majority (27 haplotypes) was found in only one individual. In contrast to previous studies on mobile insects, the overall pattern was of relatively high haplotype diversity in the absence of phylogeographic structuring.4. Migrants and non‐migrants, which sometimes shared haplotypes, were distributed across multiple genetic lineages. This suggests that, contrary to some earlier assertions, developmental pathways in this species may be plastic. Such plasticity would allow highly mobile species to adapt to a range of environmental conditions, and may be key to the widespread distribution of multiple haplotypes.

Two Anthocoris bugs as predators of glasshouse aphids – voracity and prey preference

AbstractVoracity and prey preference were evaluated for adult females of the predatory bugs Anthocoris nemorum (L.) and Anthocoris nemoralis (Fabricius) (Heteroptera: Anthocoridae) preying upon five species of aphids (Homoptera: Aphididae), of which Myzus persicae Sulzer, Aulacorthum solani (Kaltenbach), Macrosiphum euphorbiae (Thomas), and Aphis gossypii Glover are common pests in Danish glasshouse crops. Aphis fabae Scopoli was included to determine the influence of food quality on the preference of the predators, since A. fabae has proved to be of poor nutritional value to Anthocoris spp. The experiments were carried out over 24 h in climate cabinets at 20 °C, 60–70% r.h., L18:D6. The aphids were offered in equal amounts in combinations of two species in instars of comparable size. Myzus persicae served as a reference species in all combinations. Both predators accepted all five species of aphids as prey. The numbers of aphids killed per 24 h period varied between 3.7 and 18.0 for A. nemorum and between 3.6 and 12.7 for A. nemoralis. Field collected A. nemorum females, presumably in a state of reproductive diapause, killed in three of four prey combinations significantly more aphids than did ovipositing A. nemoralis females which originated from a commercial rearing. When A. nemorum females had terminated their reproductive diapause and commenced oviposition, voracity increased approximately threefold. When prey preferences were evaluated as a total number of killed prey, no difference in preference was found between the two Anthocoris species. Both predatory bugs preferred M. persicae to the other species, the most accepted alternative prey were A. gossypii, A. fabae, A. solani, and M. euphorbiae, in descending order. However, evaluating preference by number of aphids consumed, A. nemoralis showed a more pronounced preference for M. persicae, especially when combined with A. fabae. In nearly every case, A. nemoralis rejected A. fabae as a food item after killing the aphid. Thus, A. nemoralis exhibited a more specific food choice than A. nemorum. By killing and consuming different aphid species found in glasshouse crops – particularly M. persicae– both A. nemorum and A. nemoralis showed preliminary qualities as agents for the biological control of aphids.

Emergence of Overwintered Boll Weevils (Coleoptera: Curculionidae) in Relation to Microclimatic Factors

The boll weevil, Anthonomus grandis Boheman, enters a diapause state to survive winters in temperate regions and subsequently emerges from overwintering habitats to infest squaring cotton in the spring. Previous research has found that boll weevil overwintering emergence is closely associated with climatic patterns of temperature and precipitation. The objectives of this study were to determine the effects of temperature, humidity, and other meteorological factors on the temporal pattern of boll weevil emergence, and to compare the physiological and morphological conditions of emerged and trapped weevils. Emergence cages were infested with diapausing weevils in the fall. Daily emergence and microclimatic conditions of the leaf litter and air were monitored until the subsequent summer. Air temperature and relative humidity, incident solar radiation, and precipitation were significantly greater on emergence dates than on dates with no emergence. Emerged and trapped weevils were dissected to assess their morphology. Emerged weevils tended to exhibit greater fat body development, a higher frequency of testicular atrophy, and less ovary development than trapped weevils. None of the emerged weevils were rated extra lean and no trapped weevils were rated fat. These results are consistent with previously-reported effects of climatic factors on weevil emergence in other areas of the Cotton Belt, and add new information about the physiological and morphological characteristics of emerged weevils. This information on the dynamics and mechanisms of overwintering provides insight that should be helpful in formulating improved predictive models, risk assessments, and management strategies for the boll weevil.

BODY MASS AND LIPID CHANGES BY HIBERNATING REPRODUCTIVE AND NONREPRODUCTIVE BLACK BEARS (URSUS AMERICANUS)

This study, conducted on female black bears from 3 study areas in the Rocky Mountains, showed that pregnant females in a state of diapause during early winter had about 89% larger fat depots than did nonreproductive females going into hibernation. Fat provided 92% of the total energy for lactation and gestation. Rates of fat loss (g/day) were 37% greater and protein loss about 2.4 times higher for reproductive females than for nonreproductive females. The cost of winter reproduction, including gestation and lactation, was 1,432 kJ/day to produce 2 young. Although reproduction required elevated protein breakdown, rates of overall protein loss were relatively small, perhaps due to a short period of implantation and an extraordinary ability to hydrolyze urea.

Entering diapause is a prerequisite for successful cold-acclimation in adult Graphosoma lineatum (Heteroptera: Pentatomidae)

In diapause adults of Graphosoma lineatum overwintering in a field-cage, high chill-tolerance (CT) developed gradually, within 5 months from August to December. In laboratory-acclimation experiments, the diapause state appeared to be an essential pre-condition for successful cold-acclimation and overwintering. First, diapause prevented elevation of the median supercooling point (SCP) by about 5.5°C that accompanies the onset of reproductive activity in non-diapause specimens. Second, diapause allowed subsequent physiological changes resulting in cold-acclimation during a gradual (18-day) decrease of temperature from 25 to 0°C. No, or very modest, cold-acclimation was observed in non-diapause specimens. Decrease of temperature led to a rapid loss of ca. 1/3 of the body water in both non-diapause and diapause specimens. Approximately 0.1 M of trehalose accumulated in tissues of diapause specimens only, and haemolymph osmolality rose from 347 mOsm (at 25°C) to 444 mOsm after an 18-day cold-acclimation and to 764 mOsm during further storage at 0°C for 100 days. Upon transfer of cold-acclimated diapause specimens back to 25°C for one week (de-acclimation), the high CT was lost, the SCP elevated by about 2.5–3°C, and the levels of trehalose, water content and haemolymph osmolality returned to pre-acclimation or non-diapause levels.

Survival Mode between the Yearly Reproduction Periods, and Reproductive Biology of Scambus pomorum (Hymenoptera: Ichneumonidae: Pimplinae), a Parasitoid of the Apple Blossom Weevil Anthonomus pomorum (Coleoptera: Curculionidae)

First evidence is given for the hitherto unknown survival mode of females [♀♀] of the parasitoid Scambus pomorum (Ratzeburg 1848), which propagates once every spring, on larvae of the apple blossom weevil, Anthonomus pomorum Linnaeus 1758. After mating, the ♂♂ die, and the ♀♀ continue as predators of leafminer larvae, and perhaps other concealed insects, while they remain in a state of reproductive diapause. In captivity, the female parasitoids attack the mines of moths of different families, of agromyzid flies and sawflies, living on various tree species. A similar explicitly predatory life style of a parasitoid wasp has not been reported before. Leafminers as prey are not responsible for the absence of oogenesis before winter, for eggs develop in overwintered ♀♀ on the same food. Single ♀♀ kill, and feed upon, up to two Phyllonorycter blancardella (Fabricius 1781) (Lepidoptera: Gracillariidae) larvae per day at 20°C, both in early summer and autumn. Predation is linearly related to temperature. In captivity, predation by well-fed ♀♀ showed a dip in August. ♀♀ fed this way, overwintered successfully in coniferous trees, like they are known to do in nature. They became active again in late March. ♀♀ are ready to oviposit when the first suitable host stages appear, on the earliest flowering apple varieties, or on pear. One ♀ lays up to 14 eggs per day at 16.5°C, and total egg production may exceed 100 eggs, but about 50 eggs is more usual, and many ♀♀ are even less fecund. Some ♀♀ are still alive, and probably reproducing, when suitable host stages are becoming scarce. Parasitism levels should be determined when approximately 75% of the host weevils have become pupae; dissections of capped blossoms and parasitoid rearings gave similar results. Her extended lifespan makes the female wasp vulnerable to calamities like pesticide applications. Perhaps, more elevated leafminer densities in nearby hedgerows could seduce ♀♀ to leave the apple planting in time.

Juvenile hormone regulation of longevity in the migratory monarch butterfly.

Monarch butterflies (Danaus plexippus) of eastern North America are well known for their long-range migration to overwintering roosts in south-central Mexico. An essential feature of this migration involves the exceptional longevity of the migrant adults; individuals persist from August/September to March while their summer counterparts are likely to live less than two months as adults. Migrant adults persist during a state of reproductive diapause in which both male and female reproductive development is arrested as a consequence of suppressed synthesis of juvenile hormone. Here, we describe survival in monarch butterflies as a function of the migrant syndrome. We show that migrant adults are longer lived than summer adults when each are maintained under standard laboratory conditions, that the longevity of migrant adults is curtailed by treatment with juvenile hormone and that the longevity of summer adults is increased by 100% when juvenile hormone synthesis is prevented by surgical removal of its source, the corpora allatum. Thus, monarch butterfly persistence through a long winter season is ensured in part by reduced ageing that is under endocrine regulation, as well as by the unique environmental properties of their winter roost sites. Phenotypic plasticity for ageing is an integral component of the monarch butterflies' migration-diapause syndrome.

Negligible Senescence during Reproductive Dormancy inDrosophila melanogaster

Some endemic Drosophila overwinter in a state of adult reproductive diapause where egg maturation is arrested in previtellogenic stages. When maintained at cool temperatures, adult Drosophila melanogaster enter reproductive dormancy, that is, diapause or diapause-like quiescence. The ability to survive for extended periods is a typical feature of diapause syndromes. In adults this somatic persistence may involve reduced or slowed senescence. Here we assess whether reproductively dormant D. melanogaster age at slow rates. Adults were exposed to dormancy-inducing conditions for 3, 6, or 9 wk. After this period, demographic parameters were measured under normal conditions and compared to the demography of newly eclosed cohorts. The age-specific mortality rates of postdormancy adults were essentially identical to the mortality rates of newly eclosed, young flies. Postdormancy reproduction, in contrast, declined with the duration of the treatment; somatic survival during dormancy may tradeoff with later reproduction. Adults in reproductive dormancy were highly resistant to heat and to oxidative stress. Suppressed synthesis of juvenile hormone is known to regulate reproductive diapause of many insects. Treatment of dormant D. melanogaster with a juvenile hormone analog restored vitellogenesis, suppressed stress resistance, and increased demographic senescence. We conclude that D. melanogaster age at slow rates as part of their reproductive dormancy syndrome; the data do not agree with an alternative hypothesis based on heat-dependent "rate of living." We suggest that low temperature reduces neuroendocrine function, which in turn slows senescence as a function of altered stress response, nutrient reallocation, and metabolism.

Physiology of diapause and cold hardiness in the overwintering pupae of the fall webworm Hyphantria cunea (Lepidoptera: Arctiidae) in Japan

The fall webworm Hyphantria cunea Drury, which was accidentally introduced to Japan in 1945, overwinters on the ground in pupal diapause. Diapause termination, as indicated by the respiration rate and the period required for adult emergence, began in March and ended in April. Cold hardiness (the ability to survive exposure to −15°C) decreased linearly with diapause development from November to the following April under field conditions. Cold hardiness of diapause pupae (DP) decreased as the acclimation temperature decreased from 15 to −10°C, whereas cold hardiness of non-diapause pupae (NDP) remained high as the acclimation temperature decreased from 5 to −5°C. However, H. cunea in Japan can survive exposure to −5°C for two weeks, whether it is in a diapause or non-diapause state. Trehalose was the main sugar detected in the body, but its level was less than 0.8%. Trehalose levels increased in field-collected pupae from January to March. DP accumulated less trehalose than NDP, as the acclimation temperature was decreased from 5 to −5°C. The alanine content in field-collected pupae increased from November to February. Both diapause and low temperature caused an accumulation of alanine. These results suggest that under field conditions, overwintering pupae of H. cunea in Japan do not accumulate high levels of sugars and polyols and do not develop a high level of cold hardiness. Furthermore, DP do not accumulate high levels of sugars and polyols and their ability to survive exposure to −15°C is not greater than that of NDP. The physiological and biochemical bases of diapause in H. cunea from Japan are discussed.

Interaction of photoperiod and temperature in the regulation of prediapause development in the spotted tentiform leafminer (Lepidoptera: Gracillariidae)

The spotted tentiform leafminer, Phyllonorycter blancardella (F.), overwinters in a photoperiodically induced state of pupal diapause. The critical day length (50% of leafminers enter diapause) for P. blancardella from latitudes of about 42–44°N in southwestern Ontario was 14.25 h at an average August temperature (Environment Canada 1993) of 20°C (Trimble 1994). The development time of actively growing larvae decreased with increased temperature, whereas the development time of diapause-destined larvae was not affected by temperature at the critical day length, suggesting a strong interaction between photoperiod and temperature in the regulation of prediapause development (Trimble 1994). This paper describes the interaction of photoperiod and temperature in the regulation of the rate of egg and larval development of diapausedestined leafminers in the laboratory and in semi-natural conditions.

Negligible Senescence during Reproductive Dormancy in Drosophila melanogaster

Some endemic Drosophila overwinter in a state of adult reproductive diapause where egg maturation is arrested in previtellogenic stages. When maintained at cool temperatures, adult Drosophila melanogaster enter reproductive dormancy, that is, diapause or diapause‐like quiescence. The ability to survive for extended periods is a typical feature of diapause syndromes. In adults this somatic persistence may involve reduced or slowed senescence. Here we assess whether reproductively dormant D. melanogaster age at slow rates. Adults were exposed to dormancy‐inducing conditions for 3, 6, or 9 wk. After this period, demographic parameters were measured under normal conditions and compared to the demography of newly eclosed cohorts. The age‐specific mortality rates of postdormancy adults were essentially identical to the mortality rates of newly eclosed, young flies. Postdormancy reproduction, in contrast, declined with the duration of the treatment; somatic survival during dormancy may tradeoff with later reproduction. Adults in reproductive dormancy were highly resistant to heat and to oxidative stress. Suppressed synthesis of juvenile hormone is known to regulate reproductive diapause of many insects. Treatment of dormant D. melanogaster with a juvenile hormone analog restored vitellogenesis, suppressed stress resistance, and increased demographic senescence. We conclude that D. melanogaster age at slow rates as part of their reproductive dormancy syndrome; the data do not agree with an alternative hypothesis based on heat‐dependent “rate of living.” We suggest that low temperature reduces neuroendocrine function, which in turn slows senescence as a function of altered stress response, nutrient reallocation, and metabolism.

Pathogens associated with southwestern corn borers and southern corn stalk borers (Lepidoptera: Crambidae).

A study was undertaken to isolate entomopathogens of southwestern corn borer, Diatraea grandiosella Dyer, and southern corn stalk borer, Diatraea crambidoides (Grote). Field-collected diapausing larvae of southwestern corn borer (three sites in Mississippi) and southern corn stalk borer (one site in North Carolina), and a laboratory strain of D. grandiosella in the diapause state were maintained in a simulated winter followed by a simulated spring environnent. Few larvae (< or = 6%) collected from any of the field sites died in the winter environment, and most insect mortality (11-25%) occurred after transfer of the larvae to the simulated spring environment. Mortality during the simulated spring period differed among the collection sites, and the highest mortality was recorded for southwestern corn borers from Washington County (25%), followed by Marshall (16%) and Oktibbeha (11%) Counties. A high level of mortality was also observed in southern corn stalk borers during the simulated spring period (27%). No viruses were observed, but a number of bacteria, microsporidia, and fungi were isolated from both southwestern corn borer and southern corn stalk borer larvae and pupae. In most instances, numerous bacterial taxa were isolated from cadavers, but on some occasions a single taxon predominated. The most prevalent bacterial taxon from larval and pupal cadavers was Enterococcus faecalis (Andrewes & Horder) Schleifer & Kilppel-Balz, but Bacillus spp., Pseudomonas aeruginosa (Schroeter) Migula, and Serratia marcescens Bizio were frequently isolated as well. Few fungi (1-7%) were recovered from southwestern corn borer and southern corn stalk borer larvae and pupae. The most common entomopathogenic taxon isolated was Beauveria bassiana (Balsamo) Vuillemin from southern corn stalk borer larvae. Microsporidia were not isolated from southern corn stalk borers. However, Nosema spp. were isolated from southwestern corn borer cadavers from Washington (15%), Marshall (1%), and Oktibbeha (3%) Counties in Mississippi. In addition, we observed parasitism of southern corn stalk borer larvae by Macrocentrus cingulum Reinhard (Hymenoptera: Braconidae). No parasitism of southwestern corn borers was observed. Isolates of Bacillus, Beauveria, Entercoccus, Nosema, Pseudomonas and Serratia were all pathogenic to southwestern corn borer larvae under controlled environmental conditions, and with the exception of B. bassiana, these are novel pathogens of Diatraea corn borers.

Life-history variation in the coexisting freshwater copepods Eudiaptomus gracilis and Eudiaptomus graciloides

The variation in life-history patterns that allow closely related species to co-exist has been an important theme in ecology for decades. We examined intra- and interspecific variation in a key life-history trait - diapause - for two congeneric copepods (Eudiaptomus gracilis and Eudiaptomus graciloides) inhabiting three lakes in Northern Germany. Diapause has been hypothesized in both theoretical and empirical studies to be important in the coexistence of competing species. We found no diapause for E. gracilis whereas we documented two distinct periods of diapause in the life cycle of E. graciloides. In the latter species, diapausing eggs were produced in all three lakes during autumn, however, relative investment in diapausing eggs differed between lakes. Diapausing egg production was delayed or fewer females switched to making diapausing eggs in the more productive lakes relative to the less productive systems. In the sediments of all three lakes, viable diapausing eggs were found buried from the sediment-water interface down several centimeters in each lake, suggesting the presence of a long-lived egg bank. In addition, detailed population studies carried out on both species in one lake (Schohsee) revealed a second period of diapause in E. graciloides. After the diapausing eggs are produced in autumn, females accumulate lipids, reduce feeding and apparently over-winter in a state of active diapause. The prevalence of diapause in E. graciloides and lack of it in E. gracilis raises questions regarding the factors that shape the life-histories of these congeners, and the role that the life-history differences observed may play in their coexistence.

Overwintering strategies and cold hardiness of two aphid parasitoid species (Hymenoptera: Braconidae: Aphidiinae)

The role of winter diapause in two aphid parasitoid species, Aphidius ervi Haliday and Aphidius rhopalosiphi DeStefani-Peres (Hymenoptera: Braconidae: Aphidiinae), in host synchronization and the induction of cold hardiness was investigated. Parasitoids were reared during three successive generations on Sitobion avenae Fabricius, at 15°C under a photoperiod of 9 h light 15 h dark. Although these conditions are known to be strongly diapause inducing, neither parasitoids showed an incidence of diapause above 65% over the three generations; the rest of the population underwent quiescence. In both parasitoid species, diapausing mummies exhibited greater cold hardiness than non-diapausing mummies, resulting in significantly lower supercooling points (SCP) and in a higher survival rate during long-term exposures at 0 and −10°C. The induction of increased cold hardiness in parasitoids was thus associated with the diapause state. SCPs of third instar larvae of S. avenae were similar to those of non-diapausing mummies of both parasitoid species, but significantly higher than those of diapausing mummies. The effect of winter climate on the stability of the host–parasitoid interaction is discussed.

Seasonal changes in respiration rates of copepodite stage V Calanus finmarchicus (Gunnerus)

Copepodite stage V Calanus finmarchicus were collected at locations on the continental shelf north of Scotland, in the Faroe–Shetland Channel and west of Ireland on six occasions covering winter, spring and summer from October 1993 to June 1995. Oxygen consumption by the overwintering and active spring/summer population of animals was determined at temperatures close to in situ temperatures. Laboratory measurements of oxygen consumption were also made at standardized temperatures (0°C, 5°C, 7°C and 12.5°C) to determine the sensitivity of animals to temperature change in the different seasons. Rates of oxygen consumption were very low (7–30 μmol O2 gC−1 h−1) at in situ temperatures during the winter and early spring and significantly higher (105–219 μmol O2 gC−1 h−1) for the active surface population in May and June. Animals collected from the overwintering population showed no significant response to changes in temperature. Due to the low respiration rates, the calculated rate of decrease in carbon content in diapausing copepodite stage CV was very low (approximately 0.250 μgC day−1). The respiration rates were used to construct a model to estimate survival of the animals with an initial carbon content equivalent to that expected of animals in October. The results showed that in order to survive during winter and have enough energy for moulting and migration to the surface in the spring, these animals have to live at temperatures close to 0°C and be in a diapause state.

Cell Nonautonomy of C. elegans daf-2 Function in the Regulation of Diapause and Life Span

The insulin/IGF receptor homolog DAF-2 regulates the aging in C. elegans. Decreasing daf-2 activity causes fertile adults to remain active much longer than normal and to live more than twice as long. A more severe decrease in daf-2 function causes young larvae to enter a state of diapause rather than progressing to adulthood. We have asked which cells require daf-2 gene activity in order for the animal to develop to adulthood and to age normally. We found that daf-2 functions cell nonautonomously in both processes. Our findings imply that the life span of C. elegans is determined by a signaling cascade in which the DAF-2 receptor acts in multiple cell lineages to regulate the production or activity of a secondary signal (or signals), which, in turn, controls the growth and longevity of individual tissues in the animal.

Accumulation of Hsp70 mRNA under environmental stresses in diapausing and nondiapausing adults of Drosophila triauraria

Drosophila triauraria entered reproductive diapause in response to short daylengths and acquired tolerance to heat, cold and desiccation. In this species, the heat-shock response (accumulation of Hsp70 mRNA in response to heat) occurred at 27–41°C, and the level of Hsp70 mRNA did not differ between diapausing and nondiapausing individuals. Hsp70 mRNA was also induced by exposure to −4 or −8°C. However, it was scarcely detected just after the exposure to cold, but accumulated when flies were maintained at normal temperature following the exposure to cold. The level of Hsp70 mRNA was lower in diapausing individuals than in nondiapausing ones when exposed to −4°C, but was not different between them when exposed to −8°C. This species did not synthesize Hsp70 mRNA under desiccation stress irrespective of the diapause state. These results suggest that diapausing individuals of this species acquired tolerance to heat, cold and desiccation independent of the transcriptional regulation of the hsp70 gene

Characterization of the internal reproductive organs and their state as diapause indicator in Phytalus sanctipauli Blanchard, 1850 (Coleoptera, Scarabaeidae)

The internal reproductive organs of females and males of Phytalus sanctipauli are described and illustrated. The amount of fat body in the abdominal cavity was assessed. The remaining in the soil, from March to September, of sexually immature females and males bearing the abdominal cavity totally filled with fat body characterized the state of diapause in this species, in Coxilha (52°20'W and 28°05'S), RS, Brazil.

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.