Escape from parasitoids leave larvae vulnerable to predators and has unexpected outcomes for pest suppression

It is well recognised that interactions among multiple species of natural enemies can have important consequences for the population dynamics of the species involved, particularly when intra-guild predation (IGP) occurs. However, these interactions are highly dependent on the type and behaviour of the prey, an aspect of IGP that is frequently overlooked. Here we demonstrate how a parasitoid (Dolichogenidea tasmanica) facilitates attack on a lepidopteran larva (Epiphyas postvittana) by a predatory mite (Anystis baccarum). We show that anti-predator behaviour of the lepidopteran larva is the mechanism that facilitates this. E. postvittana is protected by its silken leaf roll which limits predation by the mite except when the larva is attacked by the parasitoid causing the larva to leave its shelter. We explored the implications of the interactions among these three species for pest suppression by modelling changes in mite density and mite predation intensity. The presence of mites (the IG predator) always leads to a decrease in ability of the parasitoid to control E. postvittana and, as mite predation intensity increases, the ability of the parasitoid to suppress E. postvittana decreases. The results from the experiment show a synergistic interaction, but results from the population model show an interaction resulting in pest release. These findings support the general idea that if uni-directional IGP occurs, and competition is strong between the top and intermediate predator, then a single best control agent will likely be more effective at suppressing the prey population than multiple control agents combined. These findings have important implications for the management of E. postvittana in vineyards across Southern Australia and for other multi-species systems.     

Cold tolerance of the overwintering larval instars of light brown apple moth Epiphyas postvittana

The light brown apple moth, Epiphyas postvittana, a leafroller native to southeastern Australia was discovered in California in 2006. The highly polyphagous nature of this pest adds to the importance of being able to predict the potential distribution of this invader across the North American continent. The spread of ectothermic species that lack winter diapause, such as E. postvittana, can be limited by their ability to tolerate cold temperature extremes. In this study we examined the cold hardiness of 4th to 6th instar E. postvittana, the only life stages known to overwinter in California, through a combination of supercooling point (SCP) and mortality at low temperatures. Our results showed that the mean SCP for E. postvittana ranged from −14.1 °C for 6th instars to −16.0 °C for 4th instars. Lethal time leading to 50% mortality (LT₅₀) for the three instars combined were 2.5 h at −10.5 °C, 41 h at −6.5 °C and 198 h at −0.9 °C. At 3 °C, the LT₅₀ of 4th instars was significantly lower at 775 h than that for 5th and 6th instars combined at 1029 h. The cold hardiness characteristics of later-instar E. postvittana larvae were comparable to those of pink bollworm, Pectinophora gossypiella, a diapausing invasive with a geographic distribution restricted to southern California. Slightly greater cold hardiness is shown by the indigenous non-diapausing leafroller Argyrotaenia franciscana, which is restricted to the Pacific Coast of North America. We therefore conclude that the moderate cold hardiness of E. postvittana will substantially limit its spread into northern temperate regions of North America.     

Host Plants Affect the Foraging Success of Two Parasitoids that Attack Light Brown Apple Moth Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae)

The light brown apple moth, Epiphyas postvittana is a key pest of wine grapes in Australia. Two parasitoids, Dolichogenidea tasmanica and Therophilus unimaculatus, attack the larval stage of this pest. D. tasmanica is dominant in vineyards, whereas T. unimaculatus is mainly active in native vegetation. We sought to understand why they differ in their use of habitats. Plants are a major component of habitats of parasitoids, and herbivore-infested plants influence parasitoid foraging efficiency by their architecture and emission of volatile chemicals. We investigated how different plant species infested by E. postvittana could affect the foraging success of the two parasitoid species in both laboratory and field experiments. Four common host-plant species were selected for this study. In paired-choice experiments to determine the innate foraging preferences for plants, both parasitoid species showed differences in innate search preferences among plant species. The plant preference of D. tasmanica was altered by oviposition experience with hosts that were feeding on other plant species. In a behavioral assay, the two parasitoid species allocated their times engaged in various types of behavior differently when foraging on different plant species. For both parasitoids, parasitism on Hardenbergia violacea was the highest of the four plant species. Significantly more larvae dropped from Myoporum insulare when attacked than from the other three host-plant species, which indicates that parasitism is also affected by interactions between plants and host insects. In vineyards, parasitism by D. tasmanica was significantly lower on M. insulare than on the other three host-plant species, but the parasitism rates were similar among the other three plant species. Our results indicate that plants play a role in the habitat preferences of these two parasitoid species by influencing their foraging behavior, and are likely to contribute to their distributions among habitats.     

Global Invasion of Lantana camara: Has the Climatic Niche Been Conserved across Continents?

Lantana camara, a native plant from tropical America, is considered one of the most harmful invasive species worldwide. Several studies have identified potentially invasible areas under scenarios of global change, on the assumption that niche is conserved during the invasion process. Recent studies, however, suggest that many invasive plants do not conserve their niches. Using Principal Components Analyses (PCA), we tested the hypothesis of niche conservatism for L. camara by comparing its native niche in South America with its expressed niche in Africa, Australia and India. Using MaxEnt, the estimated niche for the native region was projected onto each invaded region to generate potential distributions there. Our results demonstrate that while L. camara occupied subsets of its original native niche in Africa and Australia, in India its niche shifted significantly. There, 34% of the occurrences were detected in warmer habitats nonexistent in its native range. The estimated niche for India was also projected onto Africa and Australia to identify other vulnerable areas predicted from the observed niche shift detected in India. As a result, new potentially invasible areas were identified in central Africa and southern Australia. Our findings do not support the hypothesis of niche conservatism for the invasion of L. camara. The mechanisms that allow this species to expand its niche need to be investigated in order to improve our capacity to predict long-term geographic changes in the face of global climatic changes.     

Effect of temperature on woodwasp (Sirex noctilio F.) development and parasitism by the entomopathogenic nematode,Deladenus siricidicola

The woodwasp, Sirex noctilio, is a significant global pest of exotic pine plantations in the Southern Hemisphere and now threatens native pine forests in North America. Management in Australia relies on biocontrol using the nematode, Deladenus (= Beddingia) siricidicola (Bedding), which infects and sterilises females who then further disperse the nematode. This pest is spreading into warmer regions in Australia and South America and coupled with the threat of global climate change, there is uncertainty as to how increasing temperatures will affect the biocontrol program. S. noctilio within nematode-inoculated wood were reared at four temperatures (24, 25.3, 26.6 and 28 °C) to investigate the effects of elevated temperatures on wasp development (emergence time, sex ratio and size), development of eggs (number, size, and maturation) and infection by the nematode. At 24 °C, which reflects current field temperature, S. noctilio were bigger in size and all the eggs were normal and all were infected with nematodes. Modest rises in temperature reflecting climate change scenarios resulted in smaller sized S. noctilio, disrupted egg development and maturation, and lowered the nematode sterilisation rate in females. Reduced S. noctilio female body size and egg infection will likely compromise biocontrol by D. siricidicola in its current distribution, but disrupted egg development may act directly on the pest, limiting dispersal of S. noctilio into subtropical pine plantations and adaptation to climate change.     

Natural enemy responses and pest control: Importance of local vegetation

Natural invertebrate enemies on farmland may respond to local vegetation adjacent to the farmland. This can encourage individual landholders to maintain vegetation even when there are costs in terms of a reduction in crop area as well as maintenance of the vegetation. Here we investigated abundance of natural enemies in 61 vineyards from south eastern Australia, with either adjacent woody vegetation consisting of remnant native forests or wooded margins planted after establishment of the crop, or lacking in adjacent vegetation. Invertebrates were sampled five times at monthly intervals using canopy sticky traps. There was an increase in abundance of different groups of natural enemies when woody vegetation was present although these increases depended on size. Small natural enemies tended to be influenced by local features, whereas larger potentially more mobile groups were not affected. Predation of eggs of a vineyard insect pest, Epiphyas postvittana, was relatively higher in vineyards with either adjacent remnant forest or planted woody vegetation. Various types of local vegetation may therefore encourage a range of predators and parasitoids, increasing predation and control of a common vineyard pest.     

Establishment of a neonate cell line from Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae) that supports replication of E. postvittana nucleopolyhedrovirus

The lightbrown apple moth (Epiphyas postvittana) is a leafroller pest that damages horticultural crops in New Zealand. This paper documents the establishment of a primary cell line from neonate E. postvittana larvae to facilitate the development of E. postvittana nucleopolyhedrovirus (EppoNPV) for control of this pest. The cell line was cultured for 36 passages and a clonal derivative designated EpN1.10 was generated that had a doubling time of 36 h at 21 °C. The EpN1.10 cell line allowed for recovery of EppoNPV from transfected genomic DNA and virus passage, as determined by occlusion body production and restriction endonuclease analysis.     

The potential global distribution of the Bronze bug Thaumastocoris peregrinus Carpintero and Dellapé (Hemiptera: Thaumastocoridae)

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Could research in the native range, and non-target host range in Australia, have helped predict host range of the parasitoid Microctonus aethiopoides Loan (Hymenoptera: Braconidae), a biological control agent introduced for Sitona discoideus Gyllenhal (Coleoptera: Curculionidae) in New Zealand?

It is generally accepted that knowledge of the natural and novel host range of proposed biological control agents can help to inform predictions of potential host range in new areas of introduction. To test this hypothesis, this paper describes a retrospective study conducted to contrast and compare the natural host range of Microctonus aethiopoides Loan (Hymenoptera: Braconidae) with its novel host range found in Australia and New Zealand, where it has been introduced to control the adult stage of the weevil Sitona discoideus Gyllenhal (Coleoptera: Curculionidae), a pest of lucerne. Surveys carried out in and near lucerne crops in Morocco and Australia each resulted in collections of over 3,000 weevils, of which respectively 84?% and 93?% were S. discoideus. The host ranges determined from these surveys for each M. aethiopoides population were then compared with information already available for field host range in New Zealand. In Morocco, species in the genera Sitona and Charagmus (Curculionidae: Entiminae: Sitonini) and Hypera (Curculionidae: Hyperinae: Hyperini) were found to be parasitised by M. aethiopoides. In Australia, an earlier record of non-target parasitism of ‘Prosayleus’ sp. 2 (Curculionidae: Entiminae: Leptopiini) is still the only known instance of non-target parasitism by M. aethiopoides. The known non-target field host range in New Zealand is much greater, comprising 19 native and introduced weevil species mainly in the subfamily Entiminae (tribe Leptopiini) but also in Curculioninae, Cyclominae and Lixinae. This is discussed in the context of predictions that could have been made at the time of introduction 30?years ago had the Moroccan and Australian data, modern molecular technologies and current understanding of weevil classification been available. The absence of Leptopiini in Morocco and the record of a native Australian leptopiine host could have indicated that native weevils in this tribe in New Zealand might be at risk of attack by M. aethiopoides.     

Review of the invasion of Tetranychus evansi: biology, colonization pathways, potential expansion and prospects for biological control

In the last two decades the subtropical red tomato spider mite, Tetranychus evansi, has expanded its geographical distribution and emerged as a major invasive agricultural pest. The mite is considered to be native to South America. Since its first report from north-eastern Brazil in 1952, it has been reported from different continents. This paper reviews literature on several aspects of the biology of T. evansi related to its status as an invasive species. It addresses taxonomical issues, occurrences, life history traits, host-plant interactions, genetic diversity of geographical isolates and worldwide colonisation pathways. It also presents updated data which allowed the assessment of the actual worldwide distribution of this species, from its discovery to the latest reports. As T. evansi is considered an emerging agricultural pest, we also present data based on modelling of the potential of T. evansi to colonize new geographical areas. In addition, this review presents past and current research on natural enemies of T. evansi potentially useful for its biological control. While summarizing the knowledge on T. evansi, the review emphasizes research possibilities that are worth pursuing, mainly concerning the ability of T. evansi to establish new populations and to detect new promising natural enemies.     

Predicting the potential invasive range of light brown apple moth (Epiphyas postvittana) using biologically informed and correlative species distribution models

The light brown apple moth (Epiphyas postvittana) is a highly polyphagous species that has invaded several geographic regions across the globe and has stimulated substantial concern over possible impacts for agriculture in the US. We aimed to predict the potential geographic range of E. postvittana to better understand the threat of this species in the US and globally. We used the mechanistic simulation modelling method CLIMEX and the correlative niche modelling method Maxent to predict the geographic distribution of E. postvittana in its native range and globally and tested model projections using known invasion data. Different predictor variable data sets and threshold dependent and independent measures of environmental suitability were considered in model evaluation. Models accurately predicted known invasive localities of E. postvittana across the globe. Overall predictions of environmental suitability were largely congruent across models, although there were some notable differences. Ephiphyas postvittana clearly has the potential to establish in many regions of the globe, although some previous analyses of the potential distribution of this species appear overly pessimistic. Additional studies of the biology of this species in invaded areas, including interactions with natural enemies and the capacity to adapt to novel climatic conditions, are ultimately needed to more fully understand its potential economic and environmental impacts.     

Mate Recognition in the South African Citrus Thrips Scirtothrips aurantii (Faure) and Cross-Mating Tests with Populations from Australia and South Africa

South African citrus thrips (Scirtothrips aurantii) is a pest of citrus, mango and other horticultural species in its native range, which encompasses a large part of Africa. Its adventitious establishment in Australia in 2002 was a major cause for concern. The thrips, 11 years after its incursion into Australia, has remained on plants of a single host plant genus Bryophyllum (Crassulaceae). Characterization of the Specific-Mate Recognition System of the Bryophyllum population of thrips present in Australia and behavioral bioassay experiments revealed that compounds found in the insects’ body extracts play a crucial role in mate recognition of S. aurantii. Reciprocal cross-mating experiments between the Australian Bryophyllum insects and South African S. aurantii from horticultural host plants showed that mating frequencies were significantly lower in test crosses (Bryophyllum x horticultural) than in controls (Bryophyllum x Bryophyllum or horticultural x horticultural), which indicates there are at least two distinct species within S. aurantii and suggests further tests of this interpretation. The results suggest that these tiny phytophagous insects localize mates through their association with a particular host plant species (or closely-related group of species). Also, specific tests are suggested for clarifying the species status of the host-associated populations of S. aurantii in Africa.     

Understanding niche shifts: using current and historical data to model the invasive redlegged earth mite,Halotydeus destructor

Aim Niche conservatism is key to understanding species responses to environmental stress such as climate change or arriving in new geographical space such as biological invasion. Halotydeus destructor is an important agricultural pest in Australia and has been the focus of extensive surveys that suggest this species has undergone a niche shift to expand its invasive range inland to hotter and drier environments. We employ modern correlative modelling methods to examine niche conservatism in H. destructor and highlight ecological differences between historical and current distributions. Location Australia and South Africa. Methods We compile comprehensive distribution data sets for H. destructor, representing the native range in South Africa, its invasive range in Australia in the 1960s (40 yr post‐introduction) and its current range in Australia. Using MAXENT, we build correlative models and reciprocally project them between South Africa and Australia and investigate range expansion with models constructed for historical and current data sets. We use several recently developed model exploration tools to examine the climate similarity between native and invasive ranges and subsequently examine climatic variables that limit distributions. Results The invasive niche of H. destructor in Australia transgresses the native niche in South Africa, and the species has expanded in Australia beyond what is predicted from the native distribution. Our models support the notion that H. destructor has undergone a more recent range shift into hotter and drier inland areas of Australia since establishing a stable distribution in the 1960s. Main conclusions Our use of historical and current data highlights that invasion is an ongoing dynamic process and demonstrates that once a species has reached an established range, it may still expand at a later stage. We also show that model exploration tools help understand factors influencing the range of invasive species. The models generate hypotheses about adaptive shifts in H. destructor.     

Global variation in the piggyBac-like element of pink bollworm,Pectinophora gossypiella

The piggyBac transposable element, originally discovered in the cabbage looper, Trichoplusia ni, has been used widely in genetic engineering of insects including the pink bollworm, Pectinophora gossypiella, a major lepidopteran pest of cotton. Previously, we identified an intact copy of a piggyBac-like element (PLE) in pink bollworm, designated as PgPLE1.1. Here we report global variation in the occurrence and sequence of PgPLE1.1 and its flanking sequences. Low to high frequency of the PgPLE1.1 insertion was observed in populations from USA, Mexico, China, India, and Israel, while there is no PgPLE1.1 insertion in the populations from Australia. Investigation of the five haplotypes of PgPLE1.1, their frequency, and the flanking sequences of PgPLE1.1 revealed significant differences of the populations from Australia and China compared to other global populations, although recent occurrences of extensive gene flows among global populations were evident.     

Limits to the potential distribution of light brown apple moth in Arizona–California based on climate suitability and host plant availability

The highly polyphagous light brown apple moth (LBAM) (Epiphyas postvittana (Walk.): Tortricidae) is indigenous to Australia and was first found in California in 2006. It is currently found in 15 coastal counties in California, but nowhere has it reached outbreak status. The USDA projects the geographic range of LBAM will include much of Arizona and California and the southern half of the US, which together with economic estimates of potential crop losses have been used as the rationale for an eradication program in California. We report a temperature-driven demographic model to predict the likely distribution and relative abundance of LBAM using the detailed biology reported by Danthanarayana and colleagues, and climate data from 151 locations in California and Arizona for the period 1995–2006. The predictions of our model suggest that the near coastal regions of California are most favorable for LBAM, the northern Central Valley of California being less favorable, and the desert regions of Arizona and California being unfavorable. The model also predicts that LBAM populations can develop at two of the hottest locations in SE Australia where it is has long been known to occur. This reassessment of the potential distribution of LBAM in California and Arizona suggests that its likely ecological and economic impacts would be less than previously assessed by USDA and that its current pest status warrants re-evaluation.     

A dynamic energy budget model to describe the reproduction and growth of invasive starfish <Emphasis Type="Italic">Asterias amurensis</Emphasis> in southeast Australia

The introduction of alien species is a global phenomenon that alters ecosystems structure and functioning. Invasive species are responsible for substantial economic and ecological losses. Invasive species impact resource availability, outcompeting and even causing extinction of native species. The management of invasive species requires knowledge on the ecology, physiology and population dynamics of these species. In a world where environmental conditions are changing fast due to global climate change and other anthropogenic stressors, a more comprehensive knowledge of the life history and physiology of these species is urgently needed. The DEB theory is unique in capturing the metabolic processes of an organism through its entire life cycle, and thus, is a useful tool to model lifetime feeding, growth, reproduction, and responses to changes in biotic and abiotic conditions. In this work, we estimated the parameters of a DEB model for Asterias amurensis. This starfish was introduced in Tasmania and is considered the most serious marine pest in Australia where it has caused local extinctions of several species. Asterias amurensis is a major predator and is a keystone species exerting top-down control of its prey populations by achieving large densities. We determined the influence of biotic and abiotic factors on the performance of A. amurensis. The DEB model presented here includes energy handling rules to describe gonad and pyloric caeca cycles. Model parameters were used to explore population dynamics of populations of A. amurensis in Australia. The DEB model allowed us to characterise the ecophysiology of A. amurensis, providing new insights on the role of food availability and temperature on its life cycle and reproduction strategy. Moreover it is a powerful tool for risk management of already established invasive populations and of regions with a high invasion risk.     

A fast-track for invasion: invasive plants promote the performance of an invasive herbivore

With the greater frequency of biological invasions worldwide there is an increased likelihood that exotic species will interact with each other, and such interactions could enhance one another??s invasion potential. Although direct and indirect interactions between exotic species have been well documented for plant-herbivore interactions, the majority of studies have focused on a single interaction and on plant rather than herbivore performance. In this study we investigated whether invasive exotic plants could contribute to the invasion of California by an exotic generalist herbivore (Epiphyas postvittana). We tested this expectation in the greenhouse by monitoring the performance of larval and pupal stages of E. postvittana on six pairs of congeneric invasive and native plants. Larval survivorship and pupal weight of E. postvittana were both greater on the invasive species, and larval development time was shorter on the invasive plant species for two of the plant genera. Our results suggest that prior invasion of exotic plants could function as a catalyst for the subsequent invasion of an exotic insect herbivore, at least in the case where they have shared some history, thereby accelerating the invasion process and expansion of its novel geographic range.     

Support for the ‘out-of-Southeast Asia’ hypothesis for the origin of Australian populations of <Emphasis Type="Italic">Radopholus similis</Emphasis> (Cobb, 1893) (Nematoda: Pratylenchidae)

Radopholus similis is one of the world’s ten most economically important plant-parasitic nematodes. It is especially a problem in banana cultivation, where the nematodes’ feeding reduces yields and causes toppling disease. It has been suggested that the genus Radopholus Thorne, 1949 might have an Australian origin, but the native range of R. similis (Cobb, 1893) is not well known. Here we undertake a phylogeographical study of samples of R. similis from banana plantations down the eastern seaboard of Australia, with additional samples from Costa Rica and accessions from GenBank, to examine the origin of pest populations of R. similis. The lack of genetic diversity of R. similis within Australia, and its sharing of a worldwide pest haplotype, suggest that populations of R. similis in Australia were introduced from a single source population, most likely from the Southeast Asian region. This might not be the case in Africa, where extensive genetic diversity has been found.     

Notonomus gravis (Chaudoir) (Coleoptera: Carabidae) predation of Deroceras reticulatum Müller (Gastropoda: Agriolimacidae), an example of fortuitous biological control

The increasing use of pesticides in broad-acre cropping in South eastern Australia is suspected to have reduced native carabid beetle populations which fortuitously control potential pest populations. Slugs are increasingly becoming an establishment pest of canola, which is often attributed to stubble retention introduced to arable farming systems. Exclusion enclosures were employed to test the effect of the native carabid Notonomus gravis on the exotic pest slug Deroceras reticulatum. The native predatory species limited D. reticulatum populations and this was further supported by a negative field association between the predator and slug numbers. However, while N. gravis contributed to control of slug populations, enclosure experiments suggest that slug damage was not reduced below economic thresholds by this predator alone. Although N. gravis provides a “lying in wait” pest control option for slugs, multiple predators and environmental interactions need to be considered in developing robust integrated pest management guidelines.