Nymphal Diapause Research Articles

Bioecology of Imbrasia epimethea (Drury, 1773) caterpillars consumed in Kwilu province, Democratic Republic of the Congo

Abstract Imbrasia epimethea is one of the most esteemed and popular caterpillar species for its remarkable organoleptic and nutritional values. Its consumption extends throughout the Kwilu province and nearly the entire Democratic Republic of the Congo, but its supply is very limited. The high anthropogenic pressure and the poor harvesting techniques employed by the population of Kwilu pose a major threat to the conservation of the species. This study aims to investigate the bioecology of I. epimethea in order to develop semi-captive breeding techniques for these caterpillars, making them accessible to the population. In order to determine the host plants of I. epimethea, a survey was conducted among 424 caterpillar collectors from two populated and forested territories in the Kwilu province. To study the influence of changes in the caterpillars’ diet on their growth and determine their developmental cycle, a breeding experiment was conducted. This study revealed that the caterpillars of I. epimethea do not accept transfers from Petersianthus macrocarpus to Funtumia africana. It also confirms the polyphagy of these caterpillars while indicating that, overall, P. macrocarpus proved to be the most suitable host in the Kwilu province. I. epimethea is a social species with a development cycle, from hatching to emergence, lasting approximately 115.33 ± 3.06 days. The larval stage lasts about a month but with a prolonged period of nymphal diapause. Further analysis of the leaves of P. macrocarpus and F. africana, as well as the analysis of the caterpillars themselves, along with several breeding trials, will provide further clarification on this matter.

Diapause disruption in Cirina butyrospermi Vuillet (Lepidoptera, Attacidae), the shea caterpillar, in Burkina Faso

The shea caterpillar Cirina butyrospermi is an important insect, highly valued as a human food item in Burkina Faso. However, its appearance is seasonal due to its univoltine cycle. This study therefore investigated the possibilities of breaking the nymphal diapause by changing the environmental factors and through the hormonal treatment of prepupae and pupae using bovine insulin and 20-hydroxyecdysone. Changes in humidity and temperature did not result in emergence, suggesting a mandatory nature of the diapause in C. butyrospermi. Injection of 20-hydroxyecdysone between 20 and 40 ng on 20 C. butyrospermi pupae resulted in 15.24 and 47.5% emergence, respectively. The incubation time varied between 40 and 38 days, respectively. No emergence was observed with the injection of bovine insulin. Dipping of C. butyrospermi larvae and pupae in solutions of 20-hydroxyecdysone resulted in similar rates of emergence between the two stages, with slight variations between individual doses: (1) for larvae, emergence was recorded at 10, 8, 5 and 15 mg/l with 98.5, 62.14, 25.73 and 24.16%, respectively; the incubation times varied from 39 days at 5 mg/l to 26 days at 20 mg/l; and (2) for pupae, emergence occurred between 5 and 20 mg/l, with the highest emergence rate recorded at 10, 8 and 15 mg/l with 94.58, 65.83 and 29.58%, respectively; the incubation times varied from 53 days for the lowest dose (5 mg/l) to 37 days (20 mg/l); the best emergence rate of 94.58% coincided with an incubation time of 43 days at 10 mg/l. No emergence was observed beyond 20 mg/l in both stages. Hormonal treatment with 20-hydroxyecdysone did not affect the fecundity of C. butyrospermi, with the fecundity of artificially emerging adults overlapping with that of naturally emerging adults. The emergence rate for both was similar. These results contribute to a better understanding of the physiology of this insect, constituting a breakthrough in its sustainable use as human food.

FoxO Transcription Factor Regulate Hormone Mediated Signaling on Nymphal Diapause.

Diapause is a complex physiological adaptation phenotype, and the transcription factor Forkhead-box O (FoxO) is a prime candidate for activating many of its diverse regulatory signaling pathways. Hormone signaling regulates nymphal diapause in Laodelphax striatellus. Here, the function of the FoxO gene isolated from L. striatellus was investigated. After knocking-down LsFoxO in diapausal nymphs using RNA interference, the titers of juvenile hormone III and some cold-tolerance substances decreased significantly, and the duration of the nymphal developmental period was severely shorted to 25.5 days at 20°C under short day-length (10 L:14 D). To determine how LsFoxO affects nymphal diapause, analyses of RNA-sequencing transcriptome data after treatment with LsFoxO–RNA interference was performed. The differentially expressed genes affected carbohydrate, amino acid and fatty acid metabolism, and phosphatidylinositol 3-kinase/protein kinase B signaling pathway. Thus, LsFoxO acts on L. striatellus nymphal diapause and is, therefore, a potential target gene for pest control. This study may lead to new information on the regulation of nymphal diapause in this important pest.

Nymphal Diapause inLaodelphax striatellus(Hemiptera: Delphacidae)1

Abstract Diapause, an important developmental process in insects, is a physiological adaptation for avoiding adverse environmental conditions. Laodelphax striatellus Fallen is an important graminaceous crop pest in East Asia, and there are few reports regarding the nymphal diapause from fields with rice–wheat rotation. In the present study, we determined the fourth-instar nymph as the main diapause stage through investigation under field and laboratory conditions. Developmental duration of the third and fourth instars was longer during the short day-length (10 h light:14 h dark [10L:14D]) at 20°C than during other photoperiods. The third-instar nymph is the most sensitive stage to changes in the photoperiod. The optimal environmental factor for diapause termination was long day-length (16L:8D) at 25 to 28°C. The supercooling point was significantly reduced in diapause nymphs, and activities of trehalase, pyruvate kinase, and sorbitol dehydrogenase were significantly decreased (46.46, 37.90, and 17.64%, re...

Hormone Signaling Regulates Nymphal Diapause in Laodelphax striatellus (Hemiptera: Delphacidae)

Diapause is a physiological adaptation that allows an organism to survive adverse environmental conditions. Diapause occurs at a specific developmental stage in each species. There are few reports regarding the molecular regulatory mechanism of nymphal diapause in Laodelphax striatellus, which is an important graminaceous crop pest. Our previous studies identified the conditions for nymphal diapause in this species. Here, we combined RNA sequencing transcriptomics and quantitative proteomic analyses to identify nymphal diapause-related genes and proteins. The analysis of differentially regulated genes identified four gene/protein pairs that were synchronously up-regulated, and six gene/protein pairs that were synchronously down-regulated, suggesting that these genes may regulate nymphal diapause. The up-regulated gene juvenile hormone acid methyl transferase (JHAMT) and the down-regulated gene cytochrome P450 monooxygenase (CYP314A1, Shd) were chosen for further functional studies. After knocking-down of LsJHAMT and LsShd in vivo by RNA interference, the titer of JH III and 20E decreased significantly, and the duration of the nymphal development period was severely altered. Thus LsJHAMT and LsShd regulated JH III and 20E titers in the hemolymph to control the nymphal diapause status. This study may lead to new information on the regulation nymphal diapause of this important agricultural insect pest.

Geographic Variation of Diapause and Sensitive Stages of Photoperiodic Response inLaodelphax striatellusFallén (Hemiptera: Delphacidae)

Large numbers of the small brown planthopper Laodelphax striatellus (Fallén) (Hemiptera: Delphacidae) occur in temperate regions, causing severe losses in rice, wheat, and other economically important crops. The planthoppers enter diapause in the third- or fourth-instar nymph stage, induced by short photoperiods and low temperatures. To investigate the geographic variation in L. striatellus diapause, we compared the incidence of nymphal diapause under various constant temperature (20 and 27°C) and a photoperiod of 4:20, 8:16, 10:14, 12:12, 14:10, and 16:8 (L:D) h regimes among three populations collected from Hanoi (21.02° N, 105.85° E, northern Vietnam), Jiangyan (32.51° N, 120.15° E, eastern China), and Changchun (43.89° N, 125.32° E, north-eastern China). Our results indicated that there were significant geographic variations in the diapause of L. striatellus. When the original latitude of the populations increased, higher diapause incidence and longer critical photoperiod (CP) were exhibited. The CPs of the Jiangyan and Changchun populations were ∼12 hr 30 min and 13 hr at 20°C, and 11 hr and 11 hr 20 min at 27°C, respectively. The second- and third-instar nymphs were at the stage most sensitive to the photoperiod. However, when the fourth- and fifth-instar nymphs were transferred to a long photoperiod, the diapause-inducing effect of the short photoperiod on young instars was almost reversed. The considerable geographic variations in the nymphal diapause of L. striatellus reflect their adaptation in response to a variable environment and provide insights to develop effective pest management strategies.

Seasonal cycles in stink bugs (Heteroptera, Pentatomidae) from the temperate zone: Diversity and control

The paper reviews the diversity of seasonal cycles known in stink bugs (Heteroptera, Pentatomidae) from the temperate zone and is based on the data of 43 pentatomid species studied in detail up to date (Saulich and Musolin, 2011). All the seasonal cycles realized by pentatomids in the temperate zone can be divided into two large groups: univoltine and multivoltine cycles. In univoltine cycles, only one generation is annually realized. However, univoltinism of a particular species or population can be ensured by different mechanisms: its control can be endogenous (involving an obligate diapause) or exogenous (environmental, involving a facultative diapause). Furthermore, endogenously controlled univoltine seasonal cycles can include obligate embryonic (egg) diapause (e.g., Picromerus bidens and Apateticus cynicus), obligate nymphal diapause (e.g., Pentatoma rufipes) or obligate adult (reproductive) diapause (e.g., Palomena prasina, Palomena angulosa, and Menida scotti). Exogenously controlled seasonal cycles are more flexible. Many species that are multivoltine in the subtropical or warm temperate zones are univoltine further polewards. In this case, their univoltinism is controlled exogenously, or environmentally. The mechanism often involves such seasonal adaptations as photoperiodic response of facultative winter diapause induction with a high thermal optimum (e.g., Arma custos and Dybowskyia reticulata) or a high critical threshold of winter diapause induction response (e.g., Graphosoma lineatum). The seasonal cycles of some species include not only winter diapause (hibernation) but also summer diapause (aestivation). The diapausing stage can be the same (e.g., Nezara antennata has facultative adult winter and summer diapauses) or different (e.g., Picromerus bidens survives winter in obligate embryonic diapause and spends the hottest period of summer in facultative adult aestivation). All the multivoltine cycles follow the same general pattern, with one, two, or even more directly breeding generation(s) followed by a generation that enters winter diapause. However, this sequence may be complicated by incorporation of specific seasonal adaptations such as aestivation, migrations, different forms of seasonal polyphenism or polymorphism (e.g., seasonal changes of body color), etc. Many stink bugs demonstrate geographic clines of voltinism, producing several generations in the subtropical regions (environmentally controlled multivoltine development) and two or only one generation(s) polewards (environmentally controlled bi- or univoltinism). However, some species demonstrate a strictly bivoltine seasonal cycle: they always produce two annual generations, each with either winter or summer diapause. An example is Nezara antennata which produces two generations and enters facultative winter and summer diapauses. Semivoltine seasonal cycles last more than one year. They are not very rare among insects and are known in true bugs, but have not yet been recorded among pentatomids. Examples of different seasonal cycles are described and discussed in detail. Further discussion is focused on the ecological importance of photoperiodic and thermal responses in cases of natural or artificial dispersal of pentatomids beyond their original ranges. The phytophagous Nezara viridula and the predatory Podisus maculiventris and Perillus bioculatus are used as examples. An attempt is made to compare the phylogeny of Pentatomidae and distribution of realized patterns of their seasonal development. However, it is concluded that reconstruction of phylogenetic relationships cannot yet provide a sufficient basis for prediction of realized seasonal cycles. It is suggested that the terms uni-, bi-, multi-, and semivoltinism should refer to populations rather than species, since the realized patterns of seasonal development often differ between the northern and southern populations of the same broadly distributed species.

Discrete Modes of Life Cycle in Velarifictorus micado Species Complex (Orthoptera: Gryllidae)

Different modes of climatic adaptation often lead to a split in reproductive cohesion and stimulate speciation between populations with different patterns of life cycle. We here examined egg development and photoperiodic adaptations in the nymphal development of Velarifictorus micado. We defined fast hatching populations as nymphal diapause and slow hatching populations as egg diapause. The nymphs were reared under two photoperiods, LD 16 : 8 and LD 12 : 12 at 27.5°C, and the mean days of nymphal development were compared. The results indicate that the nymphal diapause populations showed slower nymphal development under LD 12 : 12 than under LD 16 : 8, and this retardation increased with the increase of original latitude. The egg diapause populations showed slower nymphal development under LD 16 : 8 than under LD 12 : 12. These features help synchronizing their overwintering stages. Gene flow from the opposite forms may disturb this synchronization mechanism, and therefore natural selection should favor displacement of the two forms. This could be an incipient climatic isolation mechanism of reproductive stage.

A general model for the life cycle of Dolichopoda cave crickets (Orthoptera: Rhaphidophoridae)

A general model of the Dolichopoda cave cricket life cycle was produced using RAMAS/stage simulations based on the Beverton & Holt recruitment function. The model indicates the main population parameters responsible for life cycle adjustments to ecologically different cave habitats. The lack of a uniform rate of oviposition throughout adult life, combined with egg and nymphal diapause, results in regular population growth characterized by adults emerging every two years and cohorts overlapping every other year. This pattern is common in populations living in artificial caves where the scarcity of food is likely to favour individuals that synchronise their activity with the seasonal variations in the epigean habitat. In contrast, a uniform rate of oviposition throughout adult life and no egg or nymphal diapause results in a continuous reproductive activity, and the occurrence of adults all the year round. In this case, it was not possible to distinguish between cohorts. This pattern is well represented in populations inhabiting natural caves with stable food resources. The availability of data for a population that resulted from an experimental colonization allowed us to test this model.

Nymphal diapause and its photoperiodic control in the tick Ixodes scapularis (Acari: Ixodidae).

It is shown experimentally that the option between developmental diapause and non-diapause development in nymphs of Ixodes scapularis Say, 1821 (Middle Atlantic population) is determined by photoperiodic conditions according to a two-step photoperiodic reaction of short-day long-day type. Diapause arrest of development is induced by an impact of either long day upon unfed nymphs, or short day upon engorged nymphs, while non-diapause development completed in 2-2.5 months at 20 degrees C needs the change from short-day to long-day conditions. Some ecophysiological aspects of mechanisms controlling seasonal development of ticks belonging to Ixodes ricinus complex are discussed.

Photoperiodic Control of Developmental Diapause in Nymphs of Prostriate Ixodid Ticks (Acari: Ixodidae)

Extrinsic control of developmental diapause in nymphs of prostriate ticks of the subgenus Ixodes sensu stricto (Ixodes ricinus and Ixodes persulcatus from Eurasia and Ixodes scapularis from North America) appears to be based on a complex two-step photoperiodic reaction of a short-day/long-day type. Diapause control in the subgenus Afrixodes (the South African tick Ixodes rubicundus) appears to be based on a simple long-day reaction. The option between non-diapause development and diapausing arrest in engorged nymphs is determined by both pre- and post-feeding photoperiodic regimes. Consequently diapausing arrest in engorged nymphs of Ixodes sensu stricto can be induced either by a short-day (after their engorgement) or by a long-day regime (in unfed nymphs), while active, non-diapause development is possible only when the short-day pre-feeding regime is followed by a long-day post-feeding regime. The photoperiodic response in I. (Afrixodes) rubicundus nymphs seems to be of the long-day type both before and after feeding. Consequently this non-diapause development is enabled by a long-day regime, while diapause is induced by a short-day regime of exposure. Nevertheless, there are some indications that the control of nymphal diapause in the latter species is also of a complex nature.

Ecological significance of adult summer diapause after nymphal winter diapause in Poecilocoris lewisi (Distant) (Heteroptera: Scutelleridae).

Seasonal adaptations were studied in a partially bivoltine population of Poecilocoris lewisi that overwinters as nymphs. Under short-day conditions, the final (5th) instar nymphs entered diapause, whereas under long-day conditions they emerged as adults within 2 weeks. The critical daylength for induction of the nymphal diapause was between 14 and 15 h at 25°C in the Osaka population. P. lewisi entered diapause in the adult stage also, under long-day conditions. Adults emerging in late spring started oviposition only after July. Insects transferred from long-day to short-day conditions at adult emergence began to lay eggs earlier and more synchronously than those kept continuously under long-day conditions due to prevention of the adult diapause. The critical daylength for induction of the adult diapause was also between 14 and 15 h at 25°C, as in the induction of nymphal diapause. The dogwood Cornus controversa, a principal host plant of P. lewisi, did not develop seeds until early July. Therefore, this suggests the absence of host plant seeds in late spring is the ultimate factor for the evolution of adult diapause in P. lewisi.

Pulse Rates in the Songs of Trilling Field Crickets (Orthoptera: Gryllidae: <I>Gryllus</I>)

In cricket calling songs, pulse rate is often the feature that allows females to home on the songs of conspecific males while ignoring those of other species. A previous study of the sibling species Gryllus rubens Scudder and G. texensis Cade & Otte from western Florida showed unexpected effects of developmental conditions and parental generation on the pulse rates of their songs. The current study tested for these and other effects in G. rubens from Gainesville, FL, and G. texensis from Dallas, TX. In both species, sibships from different field-fertilized females differed significantly in the effects of rearing environment on the pulse rates of their songs. Tests for effects of nymphal diapause and adult age were negative. Hybrids between the two species produced pulse rates intermediate to the rates of the control crosses. Males of G. rubens reared at 32°C produced faster pulse rates (at a standard temperature) than those reared at 25°C. Furthermore, pulse rates of field-collected males in this study and of field-collected and laboratory-reared males in the previous study increased in rough proportion to the known and estimated temperatures during nymphal development.

Flexible Life Cycle of a Cockroach Periplaneta japonica with Nymphal Diapause

A cockroach, Periplaneta japonica, is known to have a semivoltine life cycle in northern snowy areas. In the present study, nymphal development, nymphal diapause, and reproduction of a southern population were studied under laboratory and outdoor conditions to understand the life cycle strategy of this species. Nymphal development proceeded faster at a longer photoperiod, but diapause was induced at any photoperiod. The longer the photoperiod the later the nymphal instar at which diapause occurred. A sample collected early in the spring suggested that the overwintering population comprised two distinct size groups, corresponding to early and late nymphal instars. This favored the conclusion that this species requires two years to complete the life cycle, as reported for northern populations. However, by rearing cockroaches under outdoor conditions, it was found that some of the nymphs hatching early in the summer overwintered as late nymphal instars and emerged as adults in the following year. This pattern of development was observed not only in a year with an unusually hot summer but also in a year with an unusually cool summer. This species has a mixture of univoltine and semivoltine life cycles, and such a mixed voltinism appears to be adaptive for insects with a long reproductive period. The time of first oviposition was earlier at a higher temperature, but mean ovipositing interval was the shortest at around 25C and tended to be prolonged at a higher temperature. These results indicate that P. japonica is adapted to northern climates and has a highly flexible life cycle.

Diapause and seasonal life cycle strategy in the house spider, Achaearanea tepidariorum (Araneae, Theridiidae)

Abstract In order to elucidate the mechanism regulating its seasonal life cycle, the photoperiodic response of Achaearanea tepidariorum has been analysed. Nymphal development was faster in long‐day and slower in short‐day photoperiods. The combined action of low temperature, poor food supply and short daylength induced diapause at an earlier developmental stage than short days alone. Thus, photoperiod is a primary factor inducing nymphal diapause, but the diapausing instar is influenced by both temperature and food supply. Hibernating nymphs became unresponsive to photoperiod in late December. After hibernation, however, sensitivity was restored and the nymphs remained sensitive to photoperiod throughout their life. This spider could also enter an imaginal or reproductive diapause. Photoperiod was again a primary inducing factor and temperature modified the photoperiodic response to some extent. The induction of the reproductive diapause was almost temperature‐compensated whereas development was not. So the involvement of a photoperiodic counter system was suggested. Irrespective of whether the nymph had experienced diapause or not, the imaginal diapause was induced in response to a short‐day photoperiod after adult moult. Based on these observations, the seasonal life cycle and the adaptive significance of nymphal and imaginal diapause are discussed.

Life cycles of 12 species of winter stoneflies from Quebec (Plecoptera; Capniidae and Taeniopterygidae)

The life cycles of 12 species of winter stoneflies belonging to the families Capniidae and Taeniopterygidae were studied in six river systems (seven sampling sites) in southern Quebec. Eight of the cycles were previously undescribed. All species were univoltine. Adults emerged as soon as the ice broke on the streams in late winter, except for Paracapnia angulata, Taenionema atlanticum, and Strophopteryx fasciata, which emerged about 3 weeks later. The simplest cycle occurred in Paracapnia opis, and P. angulata: egg development was direct and nymphal growth proceeded steadily from May to January. All other species showed evidence of a nymphal diapause interrupting development between June and September. In Allocapnia pygmaea, A. recta, C. vernalis, Taeniopteryx maura, T. parvula, and Oemopteryx glacialis, growth was completed by January, but A. minima, A. maria, Taenionema atlanticum, and Strophopteryx fasciata continued to develop through the winter and reached maturity just before emergence. Allocapnia recta, the first species to emerge, was also the first to mature, but the population showed much variability and the last nymphs to emerge were probably the only ones to survive and reproduce under Quebec climatic conditions.

Diet and predation by three leaf‐associated stoneflies (Plecoptera) in an Arkansas mountain stream

SUMMARY. 1. Life cycles, food habits, mouthpart morphologies, prey preferences, and predator‐prey size relationships were investigated for the three most common stoneflies in leaf packs in the Little Missouri River, Arkansas: Clioperla clio (Newman), Isoperla namata Prison, and Perlesta spp. Each species was univoltine and had a fast seasonal cycle, with extended egg or nymphal diapause, rapid nymphal growth and emergence in spring to early summer.2. Foregut analysis showed predictable dietary shifts by C. clio and Perlesta spp., from detritus and diatoms in early instars to invertebrate prey in later instars. Isoperla namata fed facultatively on insects, detritus and diatoms, with no conspicuous ontogenetic shifts. The mouthparts of all three species strongly reflected their diet.3. Electivity analysis indicated opportunistic feeding by the three species, with feeding rarely differing significantly from random.4. Sizes of stonefly predators and their ingested prey were highly correlated (P<0.01). However, rather than shifting toward larger prey sizes, growing predators expanded their size thresholds and continued to include numerous small prey items in their diet. Prey choice was governed most directly by prey availability, because stoneflies selected the most abundant groups, irrespective of size or taxon.5. The likelihood of competition among the three stoneflies for prey was minimized by timing of their life cycles, differential food use and probably the temporary nature of leaf pack habitats.

Larval development and determinism of nymphal diapause in a Lepidoptera, Actias selene Hbn. (Attacidae) (author's transl)

Actias selene has been reared under different conditions of lights, photophases and temperatures. The red light (630-670 nm) corresponding to the maximum of absorption of pterobilin and phorcabilin chromoproteins reduces the average length of development from 29 days to 50 days and totally inhibits the nymphal diapause. The results are discussed.

LSD treatment of Pieris brassicae and consequences on the progeny.

AT 20° C, under white light illumination and circadian rhythm, nymphal diapause of Pieris brassicae is dependent on a short 9-h photophase. Some psychodysleptics (mesca-line sulphate and LSD), when injected during the photo-sentitive larval period, suppress diapause induction as if the larvae were subjected to a long 16-h photophase1. Abnormalities in the behaviour of the progeny of treated animals were observed. We studied them for three generations after the treatment.

EVOLUTION IN THE FIELD CRICKET, ACHETA ASSIMILIS FAB.

Progeny of northern spring field cricket adults lay non-diapause eggs, undergo nymphal diapause, and overwinter as nymphs. Progeny of northern fall adults lay diapause eggs, do not undergo nymphal diapause, and overwinter as eggs. The two populations cannot interbreed freely in the field owing to a temporal difference in breeding seasons; they did not interbreed in the laboratory. Rearing experiments show that the developmental differences are genetically based rather than environmentally conditioned, and it is, therefore, unlikely that hybrids would be viable even if they were produced in the field. Consequently these two populations behave as good species. Field crickets from Virginia developed much more rapidly than did spring crickets from Quebec. Quebec spring males and Virginia females produced hybrids with developmental rates intermediate between those of their parents. More female than male hybrids were produced, and the females developed more rapidly than did male hybrids. Offspring were produced by hybrid females and Quebec spring males, but not by hybrid females and Virginia males. Partial, but incomplete reproductive isolation exists between Quebec and Virginia field crickets. A possible mechanism of sympatric speciation in insects is discussed.