Australian Bryobia mites (Trombidiformes: Tetranychidae) form a complex of cryptic taxa with unique climatic niches and insecticide responses.

BACKGROUND: Bryobia (Koch) mites belong to the economically important spider mite family, the Tetranychidae, with >130 species described worldwide. Due to taxonomic difficulties and most species being asexual, species identification relies heavily on genetic markers. Multiple putative Bryobia mite species have been identified attacking pastures and grain crops in Australia. In this study, we collected 79 field populations of Bryobia mites and combined these with 134 populations that were collected previously. We characterised taxonomic variation of mites using 28S rDNA amplicon-based DNA metabarcoding using next-generation sequencing approaches and direct Sanger sequencing. We then undertook species distribution modelling of the main genetic lineages and examined the chemical responses of multiple field populations. RESULTS: We identified 47 unique haplotypes across all mites sampled that grouped into four distinct genetic lineages. These lineages have different distributions, with three of the four putative lineages showing different climatic envelopes, as inferred from species distribution modelling. Bryobia mite populations also showed different responses to a widely used insecticide (the organophosphate, omethoate), but not to another chemical (the pyrethroid, bifenthrin) when examined using laboratory bioassays. CONCLUSION: Our findings indicate that cryptic diversity is likely to complicate the formulation of management strategies for Bryobia mites. Although focussed on Australia, this study demonstrates the challenges of studying Bryobia and highlights the importance of further research into this complex group of mites across the world. © 2022 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Warmer temperatures reduce chemical tolerance in the redlegged earth mite (Halotydeus destructor), an invasive winter-active pest.

BACKGROUND: Quantifying how chemical tolerance of pest arthropods varies with temperature is important for understanding the outcomes of chemical control, for measuring and monitoring resistance, and for predicting how pesticide resistance will evolve under future climate change. We studied the redlegged earth mite, Halotydeus destructor (Tucker), a winter-active invasive agricultural pest in Australia. Using a replicated block experiment, we tested the effect of different thermal conditions on the expression of chemical tolerance to a pyrethroid and two organophosphates. Our chemical bioassays were conducted on two redlegged earth mite populations: one possessed organophosphate resistance, whilst the other was susceptible to pesticides. Mites were first acclimated at cool (4 °C) and warm (14 °C) conditions and then exposed to pesticides in both cool (11 °C) and warm (18 °C) test conditions. RESULTS: Warm test conditions generally reduced chemical tolerance to all pesticides relative to cool test conditions. Median lethal dose (LD50 ) values of mites tested under cool conditions were 1.12-3.57-fold greater than of mites tested under warm conditions. Acclimation had a variable and small impact on chemical responses. Thermal factors (ratio between test temperatures) were similar between populations for each active ingredient. Despite reduced chemical tolerances under warm test conditions for individual mite populations, resistance factors (ratio between resistant and susceptible mite populations) were relatively consistent. CONCLUSION: Our data provides context for prior theoretical work demonstrating climatically constrained pesticide resistances in Australian redlegged earth mites. Estimates of temperature dependent toxicity measured in this study may be useful in parameterizing models of redlegged earth mite control under an increasingly warm and more variable climate. © 2022 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Economic Injury Levels and Dynamic Action Thresholds for Diuraphis noxia (Hemiptera: Aphididae) in Australian Cereal Crops.

The Russian wheat aphid (Diuraphis noxia [Kurdjumov, Hemiptera: Aphididae], RWA) was first detected in Australia in 2016 and is threatening an annual cereal industry valued at nearly 10 billion AUD per annum. Considerable uncertainty surrounds the economic risk of D. noxia to Australian cereals, which limits cost-effective farm management decisions. Through a series of inoculated and non-inoculated field trials in 2018 and 2019 in south-eastern Australia, we generated a range of D. noxia pressure metrics under different growing conditions for barley, wheat, and durum wheat. Relative yield loss was best explained by the 'percentage of tillers with D. noxia' (%TwRWA) with 0.28% yield loss per percent of tillers with D. noxia, which is significantly lower than 0.46-0.48% for susceptible winter wheat varieties in dryland conditions in the United States. Highest infestation levels were typically reached around GS40-50. To develop an action threshold, we calculated the rate of increase in the %TwRWA through time at 0.021% per day per %TwRWA (with little variation across sites). This allowed prediction of the expected maximum %TwRWA based on observations post tillering (GS30) and the expected duration before GS50 is reached. For earlier growth stages (

Spatial Variation in Australian Neonicotinoid Usage and Priorities for Resistance Monitoring.

Australia is the third largest exporting country of cereals and a leader in other major commodity crops, yet little data exist on pesticide usage patterns in agriculture. This knowledge gap limits the management of off-target chemical impacts, such as the evolution of pesticide resistance. Here, for the first time, we quantify spatial patterns in neonicotinoid applications in Australia by coalescing land use data with sales and market research data contributed by agrichemical and agribusiness companies. An example application to resistance management is explored through the development of recommendations for the cosmopolitan crop pest, Myzus persicae (Sulzer) (Hemiptera: Aphididae), utilizing spatial statistical models. This novel dataset identified Australian neonicotinoid usage patterns, with most neonicotinoid products in Australia applied as cereal, canola, cotton and legume seed treatments and soil applications in sugarcane. Importantly, there were strong regional differences in pesticide applications, which will require regionally specific strategies to manage off-target impacts. Indeed, the estimated spatial grid of neonicotinoid usage demonstrated a statistically significant influence on the distribution of M. persicae neonicotinoid resistance, indicating off-target impacts are unevenly distributed in space. Future research on neonicotinoid usage will be supported by the spatial grids generated and made available through this study. Overall, neonicotinoid pesticides are widely relied upon throughout Australia's plant production systems but will face increasing pressure from resistance evolution, emerging research on off-target impacts, and stricter regulatory pressures.

A molecular method for biomonitoring of an exotic plant-pest: Leafmining for environmental DNA.

Understanding how invasive species respond to novel environments is limited by a lack of sensitivity and throughput in conventional biomonitoring methods. Arthropods in particular are often difficult to monitor due to their small size, rapid lifecycles, and/or visual similarities with co-occurring species. This is true for the agromyzid leafminer fly, Liriomyza sativae, a global pest of vegetable and nursery industries that has recently established in Australia. A robust method based on environmental DNA (eDNA) was developed exploiting traces of DNA left inside "empty" leaf mines, which are straightforward to collect and persist longer in the environment than the fly. This extends the window of possible diagnosis to at least 28 days after a leaf mine becomes empty. The test allowed for visually indistinguishable leafmining damage caused by L. sativae to be genetically differentiated from that of other flies. Field application resulted in the identification of new local plant hosts for L. sativae, including widely distributed weeds and common garden crops, which has important implications for the pest's ability to spread. Moreover, the test confirmed the presence of a previously unknown population of L. sativae on an island in the Torres Strait. The developed eDNA method is likely to become an important tool for L. sativae and other leafmining species of biosecurity significance, which, historically, have been difficult to detect, diagnose and monitor. More generally, eDNA is emerging as a highly sensitive and labour-efficient surveillance tool for difficult to survey species to improve outcomes for agricultural industries, global health, and the environment.

Strip spraying delays pyrethroid resistance in the redlegged earth mite, Halotydeus destructor: a novel refuge strategy.

BACKGROUND: Pesticide resistance has seen control options for the redlegged earth mite (RLEM), Halotydeus destructor, dwindle for Australian grain farmers. The recent discovery of high recessiveness for pyrethroid resistance in RLEM provided an opportunity to examine the feasibility of a refuge strategy to slow the evolution of resistance. Unlike lepidopterous pests in Bt crops, where refuge strategies are routinely practiced, RLEM is a slow-moving pest, which will impact the design of susceptible refuges. RESULTS: Firstly, we confirmed the pyrethroid resistant allele is recessive to the susceptible (wildtype) allele (in terms of resistance) across spatially separated Australian populations. Secondly, we demonstrated that a small, localized resistant mite population can revert to susceptibility at field relevant scales and conditions. Next, we used a simulation modelling approach to design a practical refuge strategy to maintain susceptibility to pyrethroids in populations with a low incidence of resistance. Certain configurations (e.g. a pesticide strip width of 50 m and refuge spacing of 10 m) maintained low levels of resistance across a 10-year time horizon, with lower mite abundance and minimal yield loss. A larger refuge proportion did not always delay resistance, and, under certain conditions, increased resistance frequency. CONCLUSION: Strip spraying to maintain refuges can be readily incorporated into RLEM management programs where sprayer widths in commercial cropping contexts are typically between 20-40 m. A refuge approach to RLEM management that uses strip spraying may enhance long term control options in the absence of new chemical registrations but will now require field validation. © 2021 Society of Chemical Industry.

Global analysis of the seasonal abundance of the invasive pest Drosophila suzukii reveal temperature extremes determine population activity potential.

BACKGROUND: The global pest spotted winged drosophila (Drosophila suzukii) continues to have a significant economic impact on fruit production in areas where it is established, in addition to newly invaded ranges. Management activities spanning national biosecurity responses to farm-scale pest control are limited by the inability to predict the timing and severity of seasonal outbreaks of D. suzukii and its climatic drivers. RESULTS: Here, we compiled and analysed data on international seasonal abundances for D. suzukii under different climates, crop types and management contexts to improve the predictability of seasonal population dynamics. In relating seasonal abundances to environmental predictors, specifically temperature, we found strong negative effects of exposure to high and low temperatures during the preceding month. Unlike most regional studies on D. suzukii phenology that focus on temperature in the physiological development range, we show that thermal extremes better explain seasonal population fluctuations. CONCLUSION: Although trap catches remain an indirect measure of infestations and must be interpreted carefully in terms of crop risk, our results should support monitoring programmes through enhanced knowledge of the climatic factors affecting D. suzukii population activity. The negative impact of high temperatures suggests that late-season management strategies focusing on manipulating crop microclimates to temperatures above 25 °C can reduce D. suzukii abundance. We show that early season abundance is modulated by climate, particularly the depth of cold extremes experienced in the preceding time interval. These associations may be further developed into early-season crop risk forecasts to support monitoring programs. © 2021 Society of Chemical Industry.

Learnings from over a decade of increasing pesticide resistance in the redlegged earth mite, Halotydeus destructor (Tucker).

BACKGROUND: The redlegged earth mite, Halotydeus destructor (Tucker), is a destructive and economically important pest of winter grain crops and pastures in Australia. It is largely controlled by pesticides, but this mite has evolved resistance to pyrethroid and organophosphate chemicals. A national Resistance Management Strategy has been developed for pro-active management to delay further resistance evolution, though its success is reliant on a detailed understanding of the incidence, patterns of spread, current distribution and the nature of resistance in the field. Here, we report on a long-term resistance surveillance programme undertaken between 2006 and 2019 informed by resistance risk forecasting. RESULTS: By mapping the Australian distribution of resistance through time, we show that resistance is present across three Australian states and covers more than 3000 km. This current range includes a recently identified population exhibiting organophosphate resistance representing the most easterly location of resistance in H. destructor. Using field history information, we identify associations for the first time between crop management practices employed by farmers and the presence of pyrethroid resistance. Management strategies that could minimize the risk of further resistance include limiting local spread of resistance through farm hygiene practices, crop rotations and reducing pesticide usage. CONCLUSION: This study highlights the challenges of resistance in H. destructor but also indicates how quantitative resistance risk analysis can be developed to target field surveillance and delay further resistance. The management strategies highlighted in this study can help maintain the effectiveness of control options but will depend on farmer engagement and adoption. © 2021 Society of Chemical Industry.

Regional and seasonal activity predictions for fall armyworm in Australia.

Since 2016, the fall armyworm (FAW), Spodoptera frugiperda, has undergone a significant range expansion from its native range in the Americas, to continental Africa, Asia, and in February 2020, mainland Australia. The large dispersal potential of FAW adults, wide host range of immature feeding stages, and unique environmental conditions in its invasive range creates large uncertainties in the expected impact on Australian plant production industries. Here, using a spatial model of population growth and spread potential informed by existing biological and climatic data, we simulate seasonal population activity potential of FAW, with a focus on Australia's grain production regions. Our results show that, in Australia, the large spread potential of FAW will allow it to exploit temporarily favourable conditions for population growth across highly variable climatic conditions. It is estimated that FAW populations would be present in a wide range of grain growing regions at certain times of year, but importantly, the expected seasonal activity will vary markedly between regions and years depending on climatic conditions. The window of activity for FAW will be longer for growing regions further north, with some regions possessing conditions conducive to year-round population survival. Seasonal migrations from this permanent range into southern regions, where large areas of annual grain crops are grown annually, are predicted to commence from October, i.e. spring, with populations subsequently building up into summer. The early stage of the FAW incursion into Australia means our predictions of seasonal activity potential will need to be refined as more Australian-specific information is accumulated. This study has contributed to our early understanding of FAW movement and population dynamics in Australia. Importantly, the models established here provide a useful framework that will be available to other countries should FAW invade in the future. To increase the robustness of our model, field sampling to identify conditions under which population growth occurs, and the location of source populations for migration events is required. This will enable accurate forecasting and early warning to farmers, which should improve pest monitoring and control programs of FAW.

A method to investigate neonicotinoid resistance in mites.

The redlegged earth mite (Halotydeus destructor) is an important agricultural pest in Australia, with a wide range of plant hosts. Halotydeus destructor has developed resistance to pyrethroid and organophosphorus insecticides as a consequence of the widespread use of these chemicals by farmers. Neonicotinoids are one of the few remaining insecticide classes registered against H. destructor in which resistance has not been detected, although there have been occasional reports of control difficulties experienced in the field. There is currently no reliable way to accurately test the response of H. destructor (or indeed any mite species) to neonicotinoid insecticides. Here, we developed a new bioassay to assess the response of mites against the neonicotinoid imidacloprid. The method provided consistent results and showed no variation when used by different operators. We generated base-line sensitivity data for imidacloprid across a number of field-collected populations of H. destructor. This is important for future monitoring of mite responses given the considerable selection pressure now being exerted across large areas of the Australian farming landscape through the widespread use of neonicotinoid seed treatments.

Summer diapause intensity influenced by parental and offspring environmental conditions in the pest mite, Halotydeus destructor.

The regulation of active and dormant stages of arthropods is critical for surviving unfavourable seasonal conditions, and for many species depends on the diapause intensity (DI). There is substantial information on diapause strategies of arthropods under winter conditions; however, most cases of summer diapause are poorly understood despite its importance in most geographic regions of the world. Here we show how complex interactions with the environment drive DI involving multiple summer diapause forms of the mite Halotydeus destructor. This invasive pest in Australia is only active in cooler months but enters diapause at the egg stage which can survive hot and dry summer conditions. Recent research points to two forms of diapause egg, a typical form with a thick chorion and a cryptic form without this chorion which is morphologically similar to non-diapause eggs. Compared with typical diapause eggs which are produced in late spring, cryptic diapause eggs could be produced together with non-diapause eggs earlier in the season with relatively cooler temperatures and shorter daylength, reflecting an advanced bet-hedging strategy. Fitness trade-offs in this strategy are investigated in this study as variability of DI of the typical and cryptic diapause forms under different environmental factors for incubating diapause eggs (temperature) and rearing parental mites (different daylength, temperature and soil moisture). With the exception of daylength, all factors impacted hatchability of diapause eggs. Higher mortality of cryptic diapause eggs indicated relatively shallower DI than typical diapause eggs, likely reflecting a fitness penalty of this bet-hedging strategy under some conditions. Hatchability of cryptic diapause eggs revealed thermal and moisture stresses have opposite and complementary effects between parental and filial generations. Although DI of filial eggs decreased in hot and dry summer conditions, parental mites reared in hotter and drier conditions increased the DI of offspring. A bet-hedging strategy involving cryptic diapause might be replaced by typical diapause under consistently stressful conditions because of higher survival, regardless of additional production costs that might be required. These findings highlight a complex set of plastic responses to summer conditions in H. destructor that undoubtedly contribute to the success of this invasive pest under a range of environments.

Escalating insecticide resistance in Australian grain pests: contributing factors, industry trends and management opportunities.

Insecticide resistance is an ever-increasing problem that threatens food production globally. Within Australia, the grain industry has a renewed focus on resistance due to diminishing chemical options available to farmers and the increasing prevalence and severity of resistance encountered in the field. Chemicals are too often used as the major tool for arthropod pest management, ignoring the potent evolutionary forces from chemical selection pressures that lead to resistance. A complex array of factors (biological, social, economic, political, climatic) have contributed to current trends in insecticide usage and resistance in the Australian grain industry. We review the status of insecticide resistance and provide a context for how resistance is currently managed. We discuss emerging technologies and research that could be applied to improve resistance management. This includes generating baseline sensitivity data for insecticides before they are launched, developing genetic diagnostics for the full complement of known resistances, expanding resistance monitoring programs, and utilizing new technologies. Additional benefits are likely to be achieved through a combination of industry awareness and engagement, risk modeling, adoption of integrated pest management tactics, greater collaboration between industry stakeholders, and policy changes around chemical use and record keeping. The Australian grain context provides lessons for other agricultural industries. © 2018 Society of Chemical Industry.

A cryptic diapause strategy in Halotydeus destructor (Tucker) (Trombidiformes: Penthaleidae) induced by multiple cues.

BACKGROUND: The polyphagous mite pest, Halotydeus destructor, typically has three generations during the cool moist season in Australia and produces over-summering diapause eggs in spring. Diapause eggs have a distinct thick and dark chorion and can survive heat, desiccation and the application of pesticides. Farmers suppress mites producing diapause eggs by a carefully timed spring pesticide application using Timerite® , which predicts the onset of diapause egg production based largely on day length. We investigated the association between diapause induction and other environmental factors that may complicate diapause predictions. RESULTS: Diapause in H. destructor induction was influenced by three interacting environmental factors, namely day length, temperature and soil moisture. A cryptic type of diapause egg that lacked a thick chorion and was instead morphologically similar to non-diapause eggs was also discovered. Like diapause eggs, this newly discovered egg type could also survive hot and dry summer conditions. CONCLUSIONS: There is an opportunity to refine the Timerite® spring spray by incorporating knowledge of other environmental factors inducing diapause in H. destructor. Compared with typical diapause eggs, the production of cryptic diapause eggs could reflect a strategy to deal with diversifying environmental stresses and/or represent a bet-hedging strategy to adapt to unpredictable environments. © 2018 Society of Chemical Industry.

Mechanistic models for predicting insect responses to climate change.

Mechanistic models of the impacts of climate change on insects can be seen as very specific hypotheses about the connections between microclimate, ecophysiology and vital rates. These models must adequately capture stage-specific responses, carry-over effects between successive stages, and the evolutionary potential of the functional traits involved in complex insect life-cycles. Here we highlight key considerations for current approaches to mechanistic modelling of insect responses to climate change. We illustrate these considerations within a general mechanistic framework incorporating the thermodynamic linkages between microclimate and heat, water and nutrient exchange throughout the life-cycle under different climate scenarios. We emphasise how such a holistic perspective will provide increasingly robust insights into how insects adapt and respond to changing climates.

Testing mechanistic models of growth in insects.

Insects are typified by their small size, large numbers, impressive reproductive output and rapid growth. However, insect growth is not simply rapid; rather, insects follow a qualitatively distinct trajectory to many other animals. Here we present a mechanistic growth model for insects and show that increasing specific assimilation during the growth phase can explain the near-exponential growth trajectory of insects. The presented model is tested against growth data on 50 insects, and compared against other mechanistic growth models. Unlike the other mechanistic models, our growth model predicts energy reserves per biomass to increase with age, which implies a higher production efficiency and energy density of biomass in later instars. These predictions are tested against data compiled from the literature whereby it is confirmed that insects increase their production efficiency (by 24 percentage points) and energy density (by 4 J mg(-1)) between hatching and the attainment of full size. The model suggests that insects achieve greater production efficiencies and enhanced growth rates by increasing specific assimilation and increasing energy reserves per biomass, which are less costly to maintain than structural biomass. Our findings illustrate how the explanatory and predictive power of mechanistic growth models comes from their grounding in underlying biological processes.

Ontogenetic and interspecific metabolic scaling in insects.

Design constraints imposed by increasing size cause metabolic rate in animals to increase more slowly than mass. This ubiquitous biological phenomenon is referred to as metabolic scaling. However, mechanistic explanations for interspecific metabolic scaling do not apply to ontogenetic size changes within a species, implying different mechanisms for scaling phenomena. Here, we show that the dynamic energy budget theory approach of compartmentalizing biomass into reserve and structural components provides a unified framework for understanding ontogenetic and interspecific metabolic scaling. We formulate the theory for insects and show that it can account for ontogenetic metabolic scaling during the embryonic and larval phases, as well as the U-shaped respiration curve during pupation. After correcting for the predicted ontogenetic scaling effects, which we show to follow universal curves, the scaling of respiration between species is approximated by a three-quarters power law, supporting past empirical studies on insect metabolic scaling and our theoretical predictions. The ability to explain ontogenetic and interspecific metabolic scaling effects under one consistent framework suggests that the partitioning of biomass into reserve and structure is a necessary foundation to a general metabolic theory.

Reconciling theories for metabolic scaling.

Metabolic theory specifies constraints on the metabolic organisation of individual organisms. These constraints have important implications for biological processes ranging from the scale of molecules all the way to the level of populations, communities and ecosystems, with their application to the latter emerging as the field of metabolic ecology. While ecologists continue to use individual metabolism to identify constraints in ecological processes, the topic of metabolic scaling remains controversial. Much of the current interest and controversy in metabolic theory relates to recent ideas about the role of supply networks in constraining energy supply to cells. We show that an alternative explanation for physicochemical constraints on individual metabolism, as formalised by dynamic energy budget (DEB) theory, can contribute to the theoretical underpinning of metabolic ecology, while increasing coherence between intra- and interspecific scaling relationships. In particular, we emphasise how the DEB theory considers constraints on the storage and use of assimilated nutrients and derive an equation for the scaling of metabolic rate for adult heterotrophs without relying on optimisation arguments or implying cellular nutrient supply limitation. Using realistic data on growth and reproduction from the literature, we parameterise the curve for respiration and compare the a priori prediction against a mammalian data set for respiration. Because the DEB theory mechanism for metabolic scaling is based on the universal process of acquiring and using pools of stored metabolites (a basal feature of life), it applies to all organisms irrespective of the nature of metabolic transport to cells. Although the DEB mechanism does not necessarily contradict insight from transport-based models, the mechanism offers an explanation for differences between the intra- and interspecific scaling of biological rates with mass, suggesting novel tests of the respective hypotheses.