Staying in touch: how highly specialised moth pollinators track host plant phenology in unpredictable climates

Background For specialised pollinators, the synchrony of plant and pollinator life history is critical to the persistence of pollinator populations. This is even more critical in nursery pollination, where pollinators are obligately dependant on female host plant flowers for oviposition sites. Epicephala moths (Gracillariidae) form highly specialised nursery pollination mutualisms with Phyllanthaceae plants. Several hundred Phyllanthaceae are estimated to be exclusively pollinated by highly specific Epicephala moths, making these mutualisms an outstanding example of plant–insect coevolution. However, there have been no studies of how Epicephala moths synchronise their activity with host plant flowering or persist through periods when flowers are absent. Such knowledge is critical to understanding the ecology and evolutionary stability of these mutualisms. We surveyed multiple populations of both Breynia oblongifolia (Phyllanthaceae) and it’s Epicephala pollinators for over two years to determine their phenology and modelled the environmental factors that underpin their interactions. Results The abundance of flowers and fruits was highly variable and strongly linked to local rainfall and photoperiod. Unlike male flowers and fruits, female flowers were present throughout the entire year, including winter. Fruit abundance was a significant predictor of adult Epicephala activity, suggesting that eggs or early instar larvae diapause within dormant female flowers and emerge as fruits mature. Searches of overwintering female flowers confirmed that many contained pollen and diapausing pollinators. We also observed diapause in Epicephala prior to pupation, finding that 12% (9/78) of larvae emerging from fruits in the autumn entered an extended diapause for 38–48 weeks. The remaining autumn emerging larvae pupated directly without diapause, suggesting a possible bet-hedging strategy. Conclusions Epicephala appear to use diapause at multiple stages in their lifecycle to survive variable host plant phenology. Furthermore, moth abundance was predicted by the same environmental variables as male flowers, suggesting that moths track flowering through temperature. These adaptations may thereby mitigate against unpredictability in the timing of fruiting and flowering because of variable rainfall. It remains to be seen how widespread egg diapause and pre-pupal diapause may be within Epicephala moths, and, furthermore, to what degree these traits may have facilitated the evolution of these highly diverse mutualisms.

Antagonism between PTP1B and PTK Mediates Adults’ Insulin-Like Signaling Regulation of Egg Diapause in the Migratory Locust

Diapause is a physiological development arrest state that helps insects to adapt to seasonality and overcome adverse environmental conditions. Numerous reports have indicated that insulinlike and fork head transcription factor (FOXO) are involved in the regulation of diapause in insects. However, the upstream modulators of the insulin-like signaling pathway (ISP) involved in diapause regulation are still unknown. Here, we used RNAi and an inhibitor to treat PTK and PTP1B in adult tissues and injected Prx V or RNAi Prx V under both short and long photoperiod conditions and monitored effects on the expression of ISP genes, the phosphorylation levels for IR and IRS, the activity of NADPH oxidase, the accumulation of reactive oxygen species (ROS) and energy metabolism, seeking to identify both proteins and broader cellular metabolism influences on diapause regulation. We found that under short photoperiod conditions PTP1B in female adults induces egg diapause, whereas PTK in female adults inhibits egg diapause. Intriguingly, we also found that the antioxidant enzyme Prx V is a negative regulator of NADPH oxidizing reaction and apparently decreases ROS production and NADPH-OX activity. In contrast, all the eggs laid by adults that were treated with a series of knockdown or purified-protein injection experiments or inhibitor studies and that were reared under long photoperiod conditions hatched successfully. Thus, our results suggest a mechanism wherein diapause-related proteins (PTP1B, PTK, and Prx V) of female adults are the upstream modulators that regulate offspring eggs’ diapause process through the insulin-like signaling pathway under short photoperiod conditions.

Maternal GABAergic and GnRH/corazonin pathway modulates egg diapause phenotype of the silkwormBombyx mori

Diapause represents a major developmental switch in insects and is a seasonal adaptation that evolved as a specific subtype of dormancy in most insect species to ensure survival under unfavorable environmental conditions and synchronize populations. However, the hierarchical relationship of the molecular mechanisms involved in the perception of environmental signals to integration in morphological, physiological, behavioral, and reproductive responses remains unclear. In the bivoltine strain of the silkwormBombyx mori, embryonic diapause is induced transgenerationally as a maternal effect. Progeny diapause is determined by the environmental temperature during embryonic development of the mother. Here, we show that the hierarchical pathway consists of a γ-aminobutyric acid (GABA)ergic and corazonin signaling system modulating progeny diapause induction via diapause hormone release, which may be finely tuned by the temperature-dependent expression of plasma membrane GABA transporter. Furthermore, this signaling pathway possesses similar features to the gonadotropin-releasing hormone (GnRH) signaling system for seasonal reproductive plasticity in vertebrates.

Bet hedging and cold-temperature termination of diapause in the life history of the Atlantic salmon ectoparasite Argulus canadensis

Argulus canadensis is a crustacean ectoparasite observed increasingly on wild migrating adult Atlantic salmon. We investigated temperature and salinity tolerance regarding development, survival and hatch of A. canadensis eggs to help understand spatiotemporal features of transmission. Argulus canadensis eggs differentiate to pharate embryos by 35 days buttheir hatch is protracted to ~7 months. Cold treatment ⩾75 days mimics overwintering and terminates egg diapause, with 84.6% (72.1–100%) metanauplius hatch induced ⩾13 °C and synchronized to 3–4 weeks. Inter- and intra-clutch variability and protracted hatch in the absence of cold-temperature termination of diapause is compatible with bet hedging. Whereas diapause likely promotes phenological synchrony for host colocalization, bet hedging could afford temporal plasticity to promote host encounter during environmental change. Our egg storage and hatch induction/synchronization methodologies can be exploited for empirical investigations. Salinity tolerance reveals both significantly higher embryonic development (94.4 ± 3.5% vs 61.7 ± 24.6%) and metanauplius hatch (53.3 ± 7.5% vs 10.1 ± 8.2%) for eggs in freshwater than at 17 ppt. Unhatched embryos were alive in freshwater by the end of the trial (213 days) but were dead/dying at 17 ppt. Eggs did not develop at 34 ppt. Salinity tolerance of A. canadensis eggs supports riverine transmission to adult Atlantic salmon during return to freshwater for mating each year.

Biology and Management of Pest Diabrotica Species in South America

The genus Diabrotica has over 400 described species, the majority of them neotropical. However, only three species of neotropical Diabrotica are considered agricultural pests: D. speciosa, D. balteata, and D. viridula. D. speciosa and D. balteata are polyphagous both as adults and during the larval stage. D. viridula are stenophagous during the larval stage, feeding essentially on maize roots, and polyphagous as adults. The larvae of the three species are pests on maize, but D. speciosa larvae also feed on potatoes and peanuts, while D. balteata larvae feed on beans and peanuts. None of these species express a winter/dry season egg diapause, displaying instead several continuous, latitude-mediated generations per year. This hinders the use of crop rotation as a management tool, although early planting can help in the temperate regions of the distribution of D. speciosa. The parasitoids of adults, Celatoria bosqi and Centistes gasseni, do not exert much control on Diabrotica populations, or show potential for inundative biocontrol plans. Management options are limited to insecticide applications and Bt genetically modified (GM) maize. Other techniques that show promise are products using Beauveria bassiana and Heterorhabditis bacteriophora, semiochemical attractants for monitoring purposes or as toxic baits, and plant resistance.

Microhabitat Variation in Egg Diapause Incidence in Summer Within a Local Population: An Adaptation to Decline in Host-Plant Suitability in Trigonotylus caelestialium (Hemiptera: Miridae)

Diapause induction in multivoltine insects is an ecophysiological event that is generally triggered by seasonal cues such as photoperiod and temperature. The rice leaf bug, Trigonotylus caelestialium (Kirkaldy), feeds on various Poaceae grasses and produces several generations a year. Previous studies have shown that adults produce diapause and nondiapause eggs under short-day and long-day conditions, respectively. However, there is a distinct mid-summer peak in diapause incidence before an autumnal increase in diapause incidence in the field, which cannot be explained by the laboratory results. The present study was performed to examine the environmental factors affecting the diapause incidence in mid-summer and the adaptive significance of this phenomenon. Seasonal trends in diapause incidence differed significantly among three sites located 150–400 m apart from each other and with different host plants. The suitability of host plants differs depending on species and seasonally. Therefore, the microhabitat difference in diapause trend is believed to be due to the difference in host plants. When field-collected female adults laying diapause eggs in late June were fed a seasonally deteriorating host (the orange foxtail, Alopecurus aequalis Sobol. [Poales: Poaceae]), they kept laying diapause eggs, whereas when fed a suitable host (the wheat, Triticum aestivum L. [Poales: Poaceae]) for 5 d, they changed oviposition mode to lay nondiapause eggs. These results indicate that host-plant suitability affects the oviposition mode of T. caelestialium. Diapause-egg oviposition in mid-summer in T. caelestialium has adaptive significance as a bet-hedging strategy against unpredictable dietary conditions.

Parental Photoperiod Affects Egg Diapause in a Montane Population of Mormon Crickets (Orthoptera: Tettigoniidae)

Insect diapause is a state of arrested development persisting when conditions are favorable for growth. Prolonged diapause, which occurs when insects remain in diapause for multiple years, is uncommon. Mormon crickets Anabrus simplex Haldane, a katydid and pest of rangeland forage and crops, were thought to be biennial in the Bighorn Mountains of Wyoming, but they are able to prolong diapause in the egg stage for multiple years. To test whether parental photoperiod serves as a cue to prolong diapause, mating pairs from the Bighorn Mountains were set in the same daily temperature and humidity profiles with 20 pairs on short daylength (12:12 [L:D] h) and 20 on long daylength (15:9 [L:D] h). Almost every parental pair had some undeveloped eggs after two warm periods. Females in short daylength were not more likely to have eggs with a biennial life cycle, but they were more likely than those in long daylength to lay eggs with multi-annual life cycles. Parents on short daylength were more likely to lay inviable eggs. Other fitness measures, such as hatchling mass, nymphal survivorship, and adult mass were not different between parental treatments. Diapause termination distributed over multiple years probably constitutes a bet-hedging strategy in an unpredictable environment.

Acridid ecology in the sugarcane agro-ecosystem in the Zululand region of KwaZulu-Natal, South Africa

Grasshoppers and locusts are well known crop and pasture pests throughout the world. Periodically they cause extensive damage to large areas of crops and grazing lands, which often exacerbate food shortage issues in many countries. In South Africa, acridid outbreaks rarely reach economic proportions, but in sugarcane plantations, localized outbreaks of native acridid species have been reported for the last eight years with increasing frequency and intensity in certain areas. This study was undertaken from May 2012 to May 2013 to identify the economically important acridid species in the sugarcane agroecosystem in these outbreak areas, to monitor seasonal activity patterns, to assess sampling methods, and to determine the pest status of the major species through damage ratings. Five acridid species of particular importance were identified: Nomadacris septemfasciata (Serville), Petamella prosternalis (Karny), Ornithacris cyanea (Stoll), Cataloipus zuluensis Sjötedt, and Cyrtacanthacris aeruginosa (Stoll). All species are univoltine. Petamella prosternalis was the most abundant species and exhibited a winter egg diapause, while N. septemfasciata, the second most abundant species, exhibited a winter reproductive diapause. Petamella prosternalis and N. septemfasciata were significantly correlated with the damage-rating index, suggesting that these two species were responsible for most of the feeding damage found on sugarcane. This study, for the first time, identified the acridid species complex causing damage to sugarcane in the Zululand area of KwaZulu-Natal, South Africa, and documented their population characteristics and related damage. These data are important information on which to base sound integrated pest management strategies.

Climate Change, Succession, and Reproductive Success of a Praying Mantid

We examined the adult phase of the Chinese praying mantid, Tenodera aridifolia sinensis (Saussure) (Mantodea: Mantidae) at the end of five growing seasons spanning two decades (1999–2018) in a successional old field. Sex ratio, which is generally male-biased by the time all members of a cohort are adults, exhibited a steady decline in proportion of males and eventual reversal by 2016, even though the calendar time of the study did not vary among years. Increasing length and warmth of the growing season resulted in earlier maturation, so we were seeing later portions of the adult phase at the same calendar time over successive years. This result is consistent with the earlier-published hypothesis that global warming can reduce fitness by warming and extending the growing season: earlier maturation results in earlier oviposition, which in turn causes eggs to hatch before onset of winter, thereby dying before egg diapause can occur. This may push the latitudinal distribution of this, and of other univoltine semelparous insects, farther north as the climate continues to warm. Reproductive output for the population, measured as total number of eggs produced by a cohort, peaked in 2004 at 8,514 and then fell to 226 by 2018, as did estimated numbers of adults. This decline was probably due to shrinkage of the open field area where prey were more abundant, by more than 2/3 as cedar trees replaced herbaceous vegetation during plant secondary succession. This is consistent with the hypothesis that succession limits the residence time in a habitat for these mantids.