Age and Density of Mated Females Affect Dispersal Strategies in Spider Mite Tetranychus ludeni Zacher.

The dispersal strategies of a species can affect its invasion success. Investigations into the dispersal strategies of invasive species in relation to different factors help improve our understanding of invasion mechanisms and provide knowledge for population management and invasion evaluation. Tetranychus ludeni Zacher (Acari: Tetranychidae) is an invasive species which is native to Europe but is now cosmopolitan. Here, we examined the effects of age and density on dispersal in mated females. Our results show that older females that are capable of producing more eggs within 24 h were more likely to disperse and moved longer distances than younger ones with fewer eggs. Older females spread most of their eggs out of their natal habitats and over longer distances, which reduced competition and increased offspring fitness. Females exhibited significantly increased dispersal probability and distances with an increase in population density to avoid crowding. The synchronization of dispersal and reproduction, along with the positive density-dependent dispersal strategy, may facilitate the habitat colonization and invasion speed of T. ludeni.

Parasitoid-host interaction behaviors in relation to host stages in the Tamarixia triozae (Hymenoptera: Eulophidae)-Bactericera cockerelli (Hemiptera: Triozidae) system.

Females of host-feeding parasitic wasps often partition hosts of different stages for feeding and parasitization, but the underlying behavioral mechanisms are largely unknown, making it difficult to evaluate parasitoid-host interactions and their effects on biological control success. Tamarixia triozae (Burks) is an ectoparasitoid of tomato-potato psyllid Bactericera cockerelli (Sulc), which utilizes nymphs and kills them both by parasitization and host feeding. In this study, we exposed female wasps to 1st- to 5th-instar psyllid nymphs simultaneously and made 13-h continuous video recording of parasitoid-host interactions. We then quantified host stage-dependent handling time for feeding and oviposition and behaviors of parasitoid attacks and host defenses from encountering to successful feeding and oviposition. Female wasps were more likely to encounter and evaluate older hosts. However, the encounter and evaluation did not necessarily result in the success of feeding and oviposition. Our findings suggest that (i) T. triozae continues to assess the host using its ovipositor after the evaluation phase, (ii) females prefer the mid-aged hosts for feeding piercing and feeding and the later instars for oviposition probing and oviposition, (iii) the combination of stage-specific host nutrition value, integument thickness and defense behavior determines the success of feeding attacks, and (iv) the optimal host resource for parasitoid offspring fitness defines host stage selection for oviposition. This study contributes to our understanding of parasitoid-host interactions and mechanisms behind host stage selections.

Pest management of postharvest potatoes: lethal, sublethal and transgenerational effects of the ectoparasitic mite Pyemotes zhonghuajia on the potato worm Phthorimaea operculella.

BACKGROUND: Potato, Solanum tuberosum, is one of the most important food crops in the world, playing a significant role in global food security. However, many potato industries and farms may suffer losses of tuber yield and quality in storage due to lepidopteran pests. Here, we evaluated the effectiveness of an ectoparasitic idiobiont mite Pyemotes zhonghuajia in the biological control of the potato tuber moth (PTM) Phthorimaea operculella by determining the lethal, sublethal (nonconsumptive) and transgenerational effects of P. zhonghuajia of various population densities and exposure durations on PTM survival, development and reproduction. RESULTS: Pyemotes zhonghuajia females were capable of killing all instar stages of PTM, while resistance to mite parasitism increased with the development of PTM life stage. The mortality of mature larvae (i.e., fourth instar) and pupae increased with increasing mite density and exposure duration. P. zhonghuajia imposed significant negative sublethal impacts on PTM pupation rate, female fecundity and adult longevity but not on immature development. The sublethal stress was transgenerational, resulting in lower reproduction in the offspring generation. CONCLUSION: P. zhonghuajia induces lethal, sublethal and transgenerational effects and significantly decreases PTM survival and reproductive out, demonstrating its high efficiency in the biological control of PTM. Our study provides insight into the mechanisms underlying the nonconsumptive effects of parasitism in an ectoparasite-host system and delivers critical information for the design and implementation of augmentative releases of P. zhonghuajia in the biological control of PTM in potato storage. © 2023 Society of Chemical Industry.

Resource allocation strategies for survival and reproduction by an invasive pest in response to intermittent fasting.

Intermittent fasting (IF) is a type of dietary restriction that involves fasting periods in intervals, which has been used as a strategy to improve health and extend longevity. Regular fasting is common during the process of biological invasions in nature. Yet, it is not clear how invasive animals adjust their resource allocations to survival and reproduction when periodical starvation occurs. Here, we used Tetranychus ludeni, a haplodiploid spider mite and an important invasive pest of horticultural crops around the world, to investigate the effects of IF on its life history strategies. We show that IF increased the longevity in females but not in males probably because of differences in resource storage, metabolic rate, and mating cost between sexes. In response to IF, females traded off fecundity and egg size but not the number of daughters for longevity gain, suggesting that T. ludeni females can adjust their life history strategies for population survival and growth during invasion process. Eggs produced by fasted females realized the same hatch rate and resultant young had the same survival rate as those by unfasted ones. In addition, IF had transgenerational maternal effects which prolonged offspring development period. We suggest that the longer immature developmental period can increase the body size of resulting adults, compensating egg size loss for offspring fitness. Our findings provide insight into resource allocations as responses to fasting, knowledge of which can be used for evaluation of pest invasions and for management of animal survival and reproduction by dietary regulations.

Temperature but Not Photoperiod Can Predict Development and Survival of an Invasive Apple Pest.

The apple leaf-curling midge, Dasineura mali Kieffer (Diptera: Cecidomyiidae), is an invasive pest of apple, and can contaminate fresh fruit for export, causing biosecurity problems. To provide crucial information for its pest risk analysis, forecast, and management, we investigated the effects of temperatures (5, 10, 15, 20 and 25 °C) and daylengths (10, 11, 12, 13, 14 and 15 h) on its development and survival. The midge eggs failed to hatch at 5 °C and larvae could not complete development at 10 °C. Pupation and emergence rates were significantly higher at 20 °C than at 15 °C and 25 °C. Daylength had no effect on these parameters. The low temperature threshold and thermal requirement to complete development from eggs to adults were 3.7 °C and 627 degree-days, respectively. The midge had a significantly lower thermal requirement for the completion of its lifecycle at 20 °C (614.5 degree-days) than at 15 °C (650.1 degree-days) and 25 °C (634.8 degree-days). The thermal model developed in this study provided accurate predictions of the number of D. mali generations and adult emergence time in each generation in different regions of New Zealand. We suggest that the model could be used to predict population dynamics of this pest in other parts of the world.

Juvenile socio-sexual experience determines lifetime sperm expenditure and adult survival in a polygamous moth, Ephestia kuehniella.

Male animals often adjust their sperm investment in response to sperm competition environment. To date, only a few studies have investigated how juvenile sociosexual settings affect sperm production before adulthood and sperm allocation during the first mating. Yet, it is unclear whether juvenile sociosexual experience (1) determines lifetime sperm production and allocation in any animal species; (2) alters the eupyrene : apyrene sperm ratio in lifetime ejaculates of any lepidopteran insects, and (3) influences lifetime ejaculation patterns, number of matings and adult longevity. Here we used a polygamous moth, Ephestia kuehniella, to address these questions. Upon male adult emergence from juveniles reared at different density and sex ratio, we paired each male with a virgin female daily until his death. We dissected each mated female to count the sperm transferred and recorded male longevity and lifetime number of matings. We demonstrate for the first time that males ejaculated significantly more eupyrenes and apyrenes in their lifetime after their young were exposed to juvenile rivals. Adult moths continued to produce eupyrene sperm, contradicting the previous predictions for lepidopterans. The eupyrene : apyrene ratio in the lifetime ejaculates remained unchanged in all treatments, suggesting that the sperm ratio is critical for reproductive success. Male juvenile exposure to other juveniles regardless of sex ratio caused significantly shorter adult longevity and faster decline in sperm ejaculation over successive matings. However, males from all treatments achieved similar number of matings in their lifetime. This study provides insight into adaptive resource allocation by males in response to juvenile sociosexual environment.

Predator- and killed prey-induced fears bear significant cost to an invasive spider mite: Implications in pest management.

BACKGROUND: The success of biological control using predators is normally assumed to be achieved through direct predation. Yet it is largely unknown how the predator- and killed prey-induced stress to prey may contribute to biological control effectiveness. Here, we investigate variations in life-history traits and offspring fitness of the spider mite Tetranychus ludeni in response to cues from the predatory mite Phytoseiulus persimilis and killed T. ludeni, providing knowledge for evaluation of the nonconsumptive contribution to the biological control of T. ludeni and for future development of novel spider mite control measures using these cues. RESULTS: Cues from predators and killed prey shortened longevity by 23-25% and oviposition period by 35-40%, and reduced fecundity by 31-37% in T. ludeni females. These cues significantly reduced the intrinsic rate of increase (rm ) and net population growth rate (R0 ), and extended time to double the population size (Dt ). Predator cues significantly delayed lifetime production of daughters. Mothers exposed to predator cues laid significantly smaller eggs and their offspring developed significantly more slowly but these eggs had significantly higher hatch rate. CONCLUSION: Predator- and killed prey-induced fears significantly lower the fitness of T. ludeni, suggesting that these nonconsumptive effects can contribute to the effectiveness of biological control to a great extent. Our study provides critical information for evaluation of biological control effectiveness using predators and paves the way for identification of chemical odors from the predator and killed prey, and development of new materials and methods for the control of spider mite pests. © 2022 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Larval social cues influence testicular investment in an insect.

Socio-sexual environment can have critical impacts on reproduction and survival of animals. Consequently, they need to prepare themselves by allocating more resources to competitive traits that give them advantages in the particular social setting they have been perceiving. Evidence shows that a male usually raises his investment in sperm after he detects the current or future increase of sperm competition because relative sperm numbers can determine his paternity share. This leads to the wide use of testis size as an index of the sperm competition level, yet testis size does not always reflect sperm production. To date, it is not clear whether male animals fine-tune their resource allocation to sperm production and other traits as a response to social cues during their growth and development. Using a polygamous insect Ephestia kuehniella, we tested whether and how larval social environment affected sperm production, testis size, and body weight. We exposed the male larvae to different juvenile socio-sexual cues and measured these traits. We demonstrate that regardless of sex ratio, group-reared males produced more eupyrenes (fertile and nucleate sperm) but smaller testes than singly reared ones, and that body weight and apyrene (infertile and anucleate sperm) numbers remained the same across treatments. We conclude that the presence of larval social, but not sexual cues is responsible for the increase of eupyrene production and decrease of testis size. We suggest that male larvae increase investment in fertile sperm cells and reduce investment in other testicular tissues in the presence of conspecific juvenile cues.

Pupal Cues Increase Sperm Production but Not Testis Size in an Insect.

Theoretic and empirical studies show that social surroundings experienced by male insects during their larval or adult stage can influence their testicular investment in diverse ways. Although insect pupae do not feed and crawl, they can communicate using sex-specific and/or non-sex specific cues. Yet, it is unknown, in any insect, whether and how male pupae can fine-tune their resource allocation to sperm production and testis size in response to socio-sexual environments. We investigated this question using a moth, Ephestia kuehniella, which produces fertile eupyrene sperm and unfertile apyrene sperm. We held male pupae individually or in groups with different sex ratios, and dissected adults upon eclosion, measured their testis size, and counted both types of sperm. We demonstrated that after exposure to conspecific pupal cues regardless of sex, male pupae increased production of eupyrenes and apyrenes at the same rate but kept testis size unchanged. We suggest that testis size is fixed after pupation because most morphological traits are formed during the larval stage, allowing little room for pupae to adjust testis size. Like adults, male pupae with fully grown testes have sufficient resources to produce more sperm of both types according to the perceived increase in sperm competition risk.

Potential Aphid Population Regulation by Aphidius colemani (Hymenoptera: Aphidiidae) in Response to Host Density, Parasitoid Density, and Age.

Aphidius colemani Viereck is an important parasitoid of green peach aphid [Myzus persicae (Sulzer)], a serious pest of greenhouse crops. Augmentation of natural enemies is the most used approach to biological control of greenhouse pests. Yet, the optimal release time, rate, and age of natural enemies are often unclear. Here we tested the influence of population density of both A. colemani and M. persicae, as well as parasitoid age, on parasitism and sex allocation. We aim is to provide information for cost-effective aphid biological control programs. We show that 1) parasitoid females increased parasitism and produced more female-biased offspring with an increase of aphid density, 2) a moderate increase of parasitoid release rate elevated parasitism and daughter production when aphid density was high, 3) parasitism rate declined with an increase of aphid density but the moderate increase of parasitoid release rate eased the decline rate, and 4) 3-d-old parasitoids parasitized more aphids than younger ones but parasitoid age had no effect on daughter production. These findings suggest that A. colemani females can adjust their ability to regulate the aphid population in response to aphid population dynamics. In augmentative programs, a moderate increase of parasitoid release when aphid density is high could achieve effective control and a release of 3-d-old parasitoids could lead to a better control outcome.

Sperm allocation strategies in a sperm heteromorphic insect.

Theories predict that in polyandrous species, the focal male should increase sperm allocation per mate in the presence of rivals to gain greater share of paternity, but in the presence of additional mates, he should reduce sperm allocation per mate to save sperm for insemination of more mates. However, empirical findings are often inconsistent and reasons behind are unclear. Furthermore, many studies use copulation duration as an estimate of the number of sperm transferred. Yet, empirical evidence for such assumption is largely lacking. Here, we used a sperm heteromorphic insect Ephestia kuehniella whose males produce two types of sperm, eupyrenes (fertile) and apyrenes (nonfertile), to test these postulations. We allowed focal males to detect chemical and acoustic but no tactile cues from rivals or additional mates both before and during mating and measured copulation duration and sperm allocation in successive copulations. We demonstrate that males transfer significantly more eupyrenes per mate in the presence of rivals and that the sperm allocation pattern persists in successive copulations under this condition. However, males do not adjust apyrene allocation in response to rivals probably because apyrenes play a relatively minor role in male reproductive success. Contrary to a previous study, focal males do not respond to additional mates most likely due to the lack of tactile cues in the present study. We reveal that sperm allocation is not a function of copulation duration in this insect for spermatophore formation and delivery occupy most of copulation duration and sperm transfer is complete near the end of copulation.

Optimizing alfalfa productivity and persistence versus greenhouse gases fluxes in a continental arid region.

Alfalfa in China is mostly planted in the semi-arid or arid Northwest inland regions due to its ability to take up water from deep in the soil and to fix atmospheric N2 which reduces N fertilizer application. However, perennial alfalfa may deplete soil water due to uptake and thus aggravate soil desiccation. The objectives of this study were (1) to determine the alfalfa forage yield, soil property (soil temperature (ST), soil water content (SWC), soil organic carbon (SOC) and soil total nitrogen (STN)) and greenhouse gas (GHG: methane (CH4), nitrous oxide (N2O), and carbon dioxide (CO2)) emissions affected by alfalfa stand age and growing season, (2) to investigate the effects of soil property on GHG emissions, and (3) to optimize the alfalfa stand age by integrating the two standard criteria, the forage yield and water use efficiency, and the total GHG efflux (CO2-eq). This study was performed in alfalfa fields of different ages (2, 3, 5 and 7 year old) during the growing season (from April to October) in a typical salinized meadow with temperate continental arid climate in the Northwest inland regions, China. Despite its higher total GHG efflux (CO2-eq), the greater forage yield and water use efficiency with lower GEIhay and high CH4 uptake in the 5-year alfalfa stand suggested an optimal alfalfa stand age of 5 years. Results show that ST, SOC and RBM alone had positive effects (except RBM had no significant effect on CH4 effluxes), but SWC and STN alone had negative effects on GHG fluxes. Furthermore, results demonstrate that in arid regions SWC superseded ST, SOC, STN and RBM as a key factor regulating GHG fluxes, and soil water stress may have led to a net uptake of CH4 by soils and a reduction of N2O and CO2 effluxes from alfalfa fields. Our study has provided insights into the determination of alfalfa stand age and the understanding of mechanisms regulating GHG fluxes in alfalfa fields in the continental arid regions. This knowledge is essential to decide the alfalfa retention time by considering the hay yield, water use efficiency as well as GHG emission.

Optimizing cold storage of the ectoparasitic mite Pyemotes zhonghuajia (Acari: Pyemotidae), an efficient biological control agent of stem borers.

Pyemotes zhonghuajia Yu, Zhang and He is a newly discovered native ectoparasitic mite that efficiently controls stem borers in China. To provide a steady and sufficient supply, extend adult lifespan and synchronize field augmentative releases of P. zhonghuajia, we determined the optimal cold storage temperature and duration by storing 1-day-old mated females at 8, 10 and 12 °C for 10-90 days with a 10-day interval in the laboratory. We then recorded mite survival during storage and monitored the post-storage reproductive performance of mites at a control temperature of 25 °C. We found that all mites survived at 10 and 12 °C for different durations, but mortality occurred when mites were stored at 8 °C for ≥ 30 days with more than 70% of mites dead when the storage duration prolonged up to 50 days. The proportion of reproductive females was higher at 10 °C but decreased with the prolonged storage duration at all test temperatures. Storage temperature had no significant effect on the pre-reproductive period and offspring sex ratio, whereas prolonged storage induced longer pre-reproductive period and lower proportion of female offspring. The reproductive period increased with increasing storage temperature and with prolonged storage up to 50 and 60 days; however, the longer reproductive period did not directly translate into greater reproductive output. We found that compared with the control, mites stored at 10 °C for up to 30 days did not significantly reduce their survival, proportion of reproductive success and number and sex ratio of offspring, suggesting that 10 °C and ≤ 30 days were the optimal cold storage temperature and duration, respectively, for post-mass production storage before the field augmentative release of P. zhonghuajia.

Insight into the success of whitefly biological control using parasitoids: evidence from the Eretmocerus warrae-Trialeurodes vaporariorum system.

BACKGROUND: Mechanisms behind the success and failure of whitefly biological control using parasitoids are largely unknown. Here we use the Eretmocerus warrae-greenhouse whitefly system to investigate how the fluctuating density of the parasitoid and its host affects three key parasitoid fitness parameters, host searching, host feeding and parasitization, providing critical knowledge for evaluation and development of whitefly biological control programmes. This is the first such study in a parasitoid-whitefly system. RESULTS: Models used and developed here show that (1) both host feeding and parasitism fit a type II functional response; (2) overall parasitoid-caused whitefly mortality significantly increases with growing density of both organisms and the parasitoid density has a significantly more positive effect; (3) with a pro-synovigenic nature, E. warrae allocate significantly more resources to parasitization than to host feeding activity in low whitefly density and high parasitoid density; and (4) low mutual interference among searching parasitoids encourages parasitoid aggregation on host patches of high density. CONCLUSION: Regardless of greenhouse whitefly density, the pest can be effectively controlled by release of E. warrae. Our study provides insight into the success of whitefly biological control programmes using the parasitoid augmentation approach. Models used and developed here can also be employed to evaluate biological control programmes for other parasitoid-whitefly systems. © 2017 Society of Chemical Industry.

Effective Biological Control Depends on Life History Strategies of Both Parasitoid and Its Host: Evidence from Aphidius colemani-Myzus persicae System.

Mechanisms behind the success and failure of aphid biological control using parasitoids are largely unknown, probably because of the lack of knowledge of life history strategies of the insects involved. Here, we measured and compared life history strategies of Myzus persicae (Sulzer) (Hemiptera: Aphididae) and its parasitoid Aphidius colemani (Viereck) (Hymenoptera: Aphidiidae), providing essential information for evaluation of the potential of A. colemani to control M. persicae. Our results show that one A. colemani female parasitized ≈220 aphids within 1 wk regardless of the aphid age. Almost all aphids parasitized at <4th instar died before reaching adulthood, and those parasitized at ≥4th instar produced very few offspring, contributing little to population growth. Although having 21% lower intrinsic rate of increase and 33% longer life cycle than the aphid, the parasitoid possessed reproductive output and net population growth rate twice as high as the aphid, and reached maximum lifetime reproductive potential 1 wk earlier than the aphid. The life history strategies reported here imply that A. colemani is potentially a good biological control agent of M. persicae. On the basis of this study, we hypothesize that immediately after the onset of M. persicae, a release rate of ≈1:220 (female parasitoid:aphids) at a weekly interval during the first 3 wk could effectively control the pest. We suggest that the success of biological control of aphids using parasitoids largely depends on life history strategies of both insects involved and time of the season when they meet.

Trade-Off Between Fitness Gain and Cost Determines Profitability of a Peach Aphid Parasitoid.

Aphidius colemani (Viereck) (Hymenoptera: Aphidiidae) is commercially produced and utilized for biological control of peach aphid Myzus persicae (Sulzer) (Hemiptera: Aphididae) on greenhouse crops in many countries. To provide knowledge for the evaluation of parasitoid-host interactions and development of effective mass rearing programs, we investigated how and why host age or size affected fitness gain in A. colemani We show that the parasitoid was significantly more likely to encounter larger hosts and that an encounter almost always triggered an attack attempt. However, the attack attempt did not proportionally translate into oviposition because larger aphids had greater ability to defend themselves and the parasitoid spent more time in handling larger aphids. The host age at parasitization had no effect on emergence rates and sex ratio of parasitoid progeny, suggesting that pupae and larvae have similar survival rate in hosts of different ages and/or the parasitoid females do not adjust sex allocation based on host size. When parasitizing mid-aged hosts, the parasitoid gained maximum fitness for their progeny in developmental period, body size, and parasitism. Taking all findings together, we suggest that parasitizing mid-aged green peach aphid nymphs is most profitable for A. colemani.

Development of a strategy for selective collection of a parasitoid attacking one member of a large herbivore guild.

Selectively collecting a single natural enemy species that parasitizes one member of a guild of herbivores that attack the same host plants can be a challenging problem during development of biological control programs. We present here a successful strategy for the collection of a strain of the egg parasitoid Avetianella longoi Siscaro (Hymenoptera: Encyrtidae), that parasitizes eggs of the longhorned borer Phoracantha recurva Newman (Coleoptera: Cerambycidae). This cerambycid is one member of a large guild of woodborers that simultaneously infest dying and fallen Eucalyptus in Australia, and it has become a major pest of Eucalyptus in many areas of the world where Eucalyptus has been introduced. Adult P. recurva of both sexes were caged on freshly cut Eucalyptus logs, and the resulting egg masses were marked and then left exposed to natural parasitization in the field. Parasitized egg masses were then harvested and held in the laboratory until adult parasitoids emerged. Parasitoids were identified as A. longoi by morphological comparisons with reference specimens, and with molecular markers. This strain of A. longoi readily accepted and had high survival rates in eggs of P. recurva. In contrast, the strain of A. longoi that has been used for biological control of P. semipunctata in California since the 1990s strongly prefers eggs of eucalyptus longhorned borer, Phoracantha semipunctata (F.) (Coleoptera: Cerambycidae), and has relatively low rates of survival to adulthood in eggs of P. recurva. The causes of these behavioral and physiological differences between the two strains are not yet known.