Identification and Risk Assessment for Worldwide Invasion and Spread of Tuta absoluta with a Focus on Sub-Saharan Africa: Implications for Phytosanitary Measures and Management

To support management decisions, molecular characterization of data and geo-reference of incidence records of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) were combined with data on the biology and ecology of the pest to estimate its climatic suitability and potential spread at regional and global scale. A CLIMEX model was developed and used for the global prediction of current and future climate-induced changes in the distributional shifts of T. absoluta. Results revealed that temperature and moisture characterized T. absoluta population growth while the pest ability to survive the cold, hot, wet and dry stress conditions are the primary characteristics defining its range frontiers. Simulated irrigation also played an important role in the model optimization. Model predictions suggest that T. absoluta represents an important threat to Africa, Asia, Australia, Northern Europe, New Zealand, Russian Federation and the United States of America (USA). Under climate change context, future predictions on distribution of T. absoluta indicated that the invasive nature of this pest will result in significant crop losses in certain locations whereas some parts of Africa may witness diminution in ranges. The following scenarios may occur: 1) T. absoluta damage potential may upsurge moderately in areas of Africa where the pest currently exists; 2) a range diminution in temperate to Sahel region with moderate upsurge in damage potential; 3) a range expansion in tropical Africa with reasonable upsurge of damage potential. These possible outcomes could be explained by the fact that the continent is already warm, with the average temperature in majority of localities near the threshold temperatures for optimal development and survival of T. absoluta. Outputs from this study should be useful in helping decision-makers in their assessment of site-specific risks of invasion and spread of T. absoluta with a view to developing appropriate surveillance, phytosanitary measures and management strategies.     

中国新发现外来入侵害虫——南美番茄潜叶蛾(鳞翅目:麦蛾科)

2017年8月,在新疆维吾尔自治区伊犁哈萨克自治州露地鲜食番茄上发现一种鳞翅目害虫,以幼虫潜食叶肉、蛀食果实,经鉴定为南美番茄潜叶蛾。该害虫原产南美洲的秘鲁,2006年入侵欧洲的西班牙,截至2017年5月,已在南美洲、欧洲、非洲、中美洲和亚洲的80多个国家和地区发生,严重危害鲜食番茄、加工番茄和樱桃番茄/圣女果,产量损失最高可达80%～100%。本文提供了南美番茄潜叶蛾的危害情况及主要形态鉴定特征,提出了防范其进一步扩散危害的措施建议以及今后应开展的主要研究方向,包括植物检疫、发生分布调查、生物学生态学特性研究、天敌资源挖掘利用等,以为积极应对南美番茄潜叶蛾对我国农业生产安全的威胁提供参考。     

New records of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) predation by Brazilian Hemipteran predatory bugs

The tomato borer Tuta absoluta, native to western South America, is an extremely devastating pest in tomato crops in most of South America, Europe and Africa North of the Sahel, causes yield losses up to 100% and decreases fruit quality in open field and greenhouse crops if control methods are not applied. In Brazil two other important lepidopteran pests – Neoleucinodes elegantalis and Helicoverpa zea – occur in tomato, as well as thrips, whiteflies and aphids. For control of these pests, frequent applications of pesticides of up to 5 times per week are needed, and these resulted in the appearance of resistant populations to a number of active ingredients and decimation of natural enemies. Biological control may offer a better, safer and more sustainable opportunity for pest management. Mirid predatory bugs are currently used with success in southern Europe to control T. absoluta and other pests. In Brazil, four Hemipteran predatory bugs, not yet known to attack T. absoluta, were found to successfully prey on eggs and larvae of this pest. The first results on their predation capacity, development, survival and reproduction on T. absoluta on tomato plants are presented.     

Biological invasion risk assessment of Tuta absoluta: mechanistic versus correlative methods

The capacity to assess invasion risk from potential crop pests before invasion of new regions globally would be invaluable, but this requires the ability to predict accurately their potential geographic range and relative abundance in novel areas. This may be unachievable using de facto standard correlative methods as shown for the South American tomato pinworm Tuta absoluta, a serious insect pest of tomato native to South America. Its global invasive potential was not identified until after rapid invasion of Europe, followed by Africa and parts of Asia where it has become a major food security problem on solanaceous crops. Early prospective assessment of its potential range is possible using physiologically based demographic modeling that would have identified knowledge gaps in T. absoluta biology at low temperatures. Physiologically based demographic models (PBDMs) realistically capture the weather-driven biology in a mechanistic way allowing evaluation of invasive risk in novel areas and climes including climate change. PBDMs explain the biological bases for the geographic distribution, are generally applicable to species of any taxa, are not limited to terrestrial ecosystems, and hence can be extended to support ecological risk modeling in aquatic ecosystems. PBDMs address a lack of unified general methods for assessing and managing invasive species that has limited invasion biology from becoming a more predictive science.

     

Suitability of the tomato borer Tuta absoluta as prey for Macrolophus pygmaeus and Nesidiocoris tenuis

The tomato borer, Tuta absoluta (Meyrick) (Lep.: Gelechiidae), is an important tomato pest native to South America, which appeared in eastern Spain at the end of 2006. Prey suitability of T. absoluta eggs and larval instars was examined under laboratory conditions to evaluate whether two indigenous predators, Macrolophus pygmaeus (Rambur) and Nesidiocoris tenuis Reuter (Hem.: Miridae), can adapt to this invasive pest. Both predators preyed actively on T. absoluta eggs and all larval stages, although they preferred first‐instar larvae. Our results demonstrate that both mirids can adapt to this invasive pest, contributing to their value as biological control agents in tomato crops.     

Assessing European Egg Parasitoids as a Mean of Controlling the Invasive South American Tomato Pinworm Tuta absoluta

The South American tomato pinworm (Tuta absoluta) has recently invaded Europe and is rapidly spreading in the Afro-Eurasian continent where it is becoming a major pest on tomato crops. Laboratory tests were undertaken to evaluate the potential of 29 European strains of Trichogramma parasitoids to control T. absoluta. In addition to the host itself, the host plant (tomato) was used during the laboratory tests in order to increase the chance of selecting the best parasitoid strains. Trichogramma females were placed with T. absoluta eggs on a tomato leaflet in tubes. We compared the parasitism of T. absoluta by the various Trichogramma species tested to the Trichogramma species currently commercially available for the pest control in Europe, i.e. Trichogramma achaeae. Thereafter, the more promising strains were tested on a larger scale, in mesocosm (i.e. cages in greenhouses) and in greenhouse compartments to evaluate efficiency of laboratory selected strains under cropping conditions. The most efficient strain from the laboratory screening trials did not perform as efficiently under the greenhouse conditions. We discuss differences in parasitism levels among species and strains and among the different scales tested in the experiments, as well as implications of these results for further screening for biocontrol agents.     

Natural enemies of Tuta absoluta in the Mediterranean basin,Europe and South America

The tomato leafminer Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) represents a global threat to commercial tomato (Solanum lycopersicum L.) production, both in open field and greenhouse. Native to South America, it spread over the Mediterranean Basin, Europe, Africa and part of Asia in only 12 years, and currently it is reported in over 80 countries. Biological control is one of the options for its control and a large number of natural enemies has been reported in association with the pest, both in the areas of origin and of introduction. The egg parasitoid Trichogramma pretiosum, in South America, and the mirid predators Macrolophus pygmaeus and Nesidiocoris tenuis, in Europe and the Mediterranean basin, are used as commercial biocontrol agents. Even if several natural enemies might be promising candidates for biocontrol, their potential role in quantitative pest reduction has been seldom established under practical tomato production conditions.

Since climatic suitability indices predict a high probability for continued invasion by T. absoluta, mainly in China and the USA, there is an urgent need for new control options. In order to minimise the use of broad spectrum insecticides, biocontrol techniques should be considered. As tomato is produced seasonally, augmentative biocontrol seems to be the most effective control option, but pest reduction might be optimised by adding conservation biocontrol, and by combining biocontrol within IPM programmes.

Here, an overview of predators and parasitoids of T. absoluta in South American and Euro-Mediterranean regions, and their biological control efficacy under laboratory, semi-field and field conditions is provided.     

Assessment of Tuta absoluta yield loss in Iranian tomato crops

The South American tomato pinworm, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae), a devastating pest of tomato plants, originates from South America but it has been considered an invasive pest for Iran since 2010. To assess crop loss caused by this pest, a study was conducted in a 600 m² field under a randomised complete block design. The impact of different initial densities of T. absoluta, including control (without infestation), one, two, four, and eight T. absoluta eggs on each host plant in the first and second year was investigated with an additional treatment (16 pinworm eggs per host plant) used in the second year. Yield attributes including length and width of fruits, numbers of infested and intact fruits along with their weights were sampled and assessed on a weekly basis. In addition, the correlation between the number of galleries and these characteristics was also investigated. Crop loss data demonstrated that the effect of different infestation levels on fruit size and the weight of intact fruits was not significant over both years. However, the effect of treatment on the percentage and weight of infested fruits was shown to be significantly different in 2014 and 2015. Furthermore, there was a negative significant correlation between the number of galleries and weight of infested fruits in both years. Collectively, these results will be useful for enhancing pest management programs of T. absoluta in Iran.     

世界毁灭性检疫害虫番茄潜叶蛾的生物生态学及危害与控制

番茄潜叶蛾原产于南美洲的秘鲁,严重危害多种茄科作物,是最具毁灭性的世界检疫性害虫,严重发生地块番茄减产80%~100%。该虫主要借助农产品的贸易活动进行远距离传播扩散。截至2017年,番茄潜叶蛾已在全世界的85个国家和地区发生(以及在22个国家和地区疑似发生)。目前,我国尚没有该虫分布,然而其一旦入侵,将对我国的番茄和马铃薯产业构成巨大威胁。从番茄潜叶蛾寄主范围、危害特点及造成的经济损失、生物生态学习性、地理分布和传播扩散途径、防控措施等方面进行概述,以期为该虫的有效防范提供参考。     

Susceptibility of Cypriot Tuta absoluta populations to four targeted insecticides and control failure likelihood

Tuta absoluta, known as the South American tomato pinworm, is one of the most disastrous pests of tomato cultivations, presently menacing tomato cultivations worldwide. In 2006, T. absoluta invaded Spain from South America. Since then, it was rapidly spread to most European, African and Asian countries. Such alien invasive species can minimize crop production, whereas the increasing use of insecticides raises various environmental concerns as well as on control costs, control failure and the toxicity to non‐target organisms. The S. American tomato pinworm is mostly controlled by chemical insecticides, and failure to control it is not a rare phenomenon. Resistance to numerous insecticides has been reported and is mainly due to the fact that farmers do not follow a sustainable resistance management scheme. Several examples have been reported from several countries where the tomato pinworm is present. In order to develop a successful insecticide resistance management (IRM) strategy for any major pest, one needs to identify the baseline toxicity to insecticides and then monitor susceptibility levels . In Cyprus, the current status of susceptibility levels to the main insecticides that are used to control T. absoluta has never been studied before. Herein, nine Cypriot populations of the pest were subjected to laboratory bioassays between 2016 and 2018 using the main insecticides applied against it. We found that the insecticides chlorantraniliprole and indoxacarb could not control the Cypriot T. absoluta populations anymore, with a resistance ratio (RR) >28 and 3–23, respectively. Furthermore, mortality achieved by those two insecticides was 20.6%–72% for chlorantraniliprole and 27.5%–78% for indoxacarb. However, the insecticides emamectin benzoate and spinosad are very effective, since mortality to both of them ranged between 99.5% and 100%.     

Invasion dynamics of Lantana camara L. (sensu lato) in South Africa

Lantana camara L. (sensu lato) has a wide range of impacts throughout its global invasive range. Here we review the mechanisms driving its invasion dynamics in South Africa at national (biome, habitat) and regional (within a protected area) scales. Although only three introduction events into South Africa have been recorded (the earliest in 1858), as of 1998 L. camara was found in over 2 million ha (total area), with a condensed area of about 70,000 ha. Moreover, L. camara is present in most of the country's major biomes and a diversity of habitats, confirming its broad ecological tolerance. Using correlative bioclimatic models, we show that under future climate conditions, L. camara's range in South Africa could expand considerably over the coming decades. While human-mediated dispersal and climatic suitability have been crucial in shaping L. camara's current broad-scale distribution in South Africa, dispersal by birds and along rivers are important drivers of invasion at landscape scales. For example, current evidence suggests that in the Kruger National Park, L. camara has spread primarily along rivers. We conclude with a discussion on the implications of the different invasion dynamics for biological control and management, and provide recommendations for future research.     

Native parasitoids associated with Tuta absoluta in the tomato production areas of the Spanish Mediterranean Coast

The tomato borer Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) is an invasive pest that produces significant damage to tomato crops in the Mediterranean area. Although several species of predatory bugs are successfully being used for biological control of the pest, little is known about the parasitoids that are able to exploit T. absoluta as a host. With the aim of better understanding parasitoid species richness of T. absoluta along the Mediterranean Spanish Coast, we conducted an extensive survey to determine distribution, host plants and habitats where parasitoids are present. Our results indicated that egg parasitoids are naturally scarce but that the species richness of larval/pupal parasitoids is high and includes 20 different species. Seven of these had not been previously reported as T. absoluta parasitoids. The most frequent parasitoid species recovered were Necremnus sp. nr. artynes (Walker), Stenomesius cf. japonicus (Ashmead) and Neochrysocharis formosa (Westwood) (Hymenoptera: Eulophidae).     

Sharing a predator: can an invasive alien pest affect the predation on a local pest?

Invasive species can strongly affect biotic interactions in ecosystems, interacting both directly and indirectly with local species. In European tomato greenhouses, the invasive alien pest Tuta absoluta may impact the population dynamics of other pests like whiteflies. Besides inducing damages to the host plant and competing for resources with local pests, this alien species may exert a predator-mediated interaction on local pests sharing common natural enemies. Biocontrol agents usually used against whiteflies may also prey upon T. absoluta and this could alter the dynamics of local pest populations. We evaluated possible resource competition and predator-mediated interactions in a system involving one mirid predator Macrolophus pygmaeus and two pests, T. absoluta and a local whitefly, Bemisia tabaci, on greenhouse tomatoes. Results showed that both resource competition and predator-mediated interactions occurred simultaneously. In the presence of the shared predator, there was a short-term positive effect of T. absoluta on B. tabaci [up to 5.9-fold increase of B. tabaci juveniles (egg + larvae) after four weeks]. However, in the long-term there was a negative predator-mediated interaction of T. absoluta on B. tabaci, i.e., after ten weeks the density of B. tabaci was 7.3-fold lower in the presence of the invasive pest. We emphasize the critical role of generalist predators in managing both local and invasive alien pest populations and that the strength and direction of predator-mediated indirect interactions can depend on the time scale considered.     

The entomopathogen Beauveria bassiana has epiphytic and endophytic activity against the tomato leaf miner Tuta absoluta

The recent introduction and rapid spread of the tomato leaf miner Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) throughout Europe, Africa and the Middle East poses a severe threat to future cultivation of tomato and other Solanaceae. Among the best practicable means for effective and sustainable control of this invasive insect pest are entomopathogenic fungi, which can either prevent a further spread of this insect to new areas or keep population densities below an economic threshold level. Here, we report on the efficacy of a commercially available mycoinsecticide based on the entomopathogen Beauveria bassiana (Bals.) Vuill. (Ascomycota: Hypocreales) against all four larval stages of T. absoluta. In bioassays, high mortality rates and significantly reduced longevity of larvae were obvious when larvae had fed for a period of around 15 days on leaves with B. bassiana propagules present on the surface as an epiphyte with mortality values corrected for variance in control mortality of 90–100%. In addition, a second mode of action of B. bassiana against T. absoluta larvae was evident in bioassays in the form of an endophytic establishment of this fungus in treated tomato plants. Longevity of T. absoluta L4 larvae was significantly lower in individuals which had fed on surface‐sterilized tomato leaves obtained from plants treated 18 days before the bioassay with a B. bassiana suspension compared to larvae feeding on control plants treated with water. Corrected mortality reached values between 30% and 50% for all larval instars. Growth of tomato plants was not inhibited due to colonization by endophytic B. bassiana and a weak systemic translocation of fungal propagules in non‐treated leaves was evident in the assays. Accordingly, entomopathogenic fungi like B. bassiana express different modes of action again target insect pests, which is of particular relevance for the design of efficient management strategies for invasive pests like T. absoluta.     

Where are the seeds? Lack of floral morphs prevent seed production by the tristylous Pontederia cordata in South Africa

Reproduction is a crucial part of the successful establishment and spread of an invasive species. Invasive plants often produce seeds prolifically to spread into new ranges, yet the invasive macrophyte, Pontederia cordata L., does not appear to produce seeds in South Africa, limiting its invasive potential. Here, we aimed to determine what limits seed production of the tristylous P. cordata in South Africa, where it is widespread with impacts on the ecology of wetlands it invades, South Africa. We measured floral traits and pollen grain size from populations throughout the invasive range in South Africa to determine the relative proportion of tristylous morphs. We speculated that the absence of specialist native pollinators in the invasive range may be responsible for the absence of sexual reproduction and thus conducted a pollination study to determine whether flowers were visited. Thereafter, we hand pollinated 8865 flowers to conclude whether P. cordata exhibited an incompatibility system, which prevented seed production. The floral traits and pollen grain measurements were similar to those reported for short‐morphed flowers from the native range. The pollination study confirmed the absence of specialist insect visitors, while the hand‐pollination experiments resulted in no seed production. Only short‐morphed plants are present in South Africa, and the illegitimate pollination of short‐morphed plants prevents seed production. Vegetative spread through rhizome production is thus responsible for the invasion of P. cordata throughout South Africa. These findings suggest that control programs should target the plants'' rhizomes to prevent and reduce spread. More importantly, preventing the introduction of medium‐ and long‐morphed plants into South Africa is crucial to preclude P. cordata from producing seeds and enhancing invasion.     

Insecticide susceptibility level and control failure likelihood estimation of Sub-Saharan African populations of tomato leafminer: Evidence from Burkina Faso

The South American tomato pinworm, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) is a leafminer species currently considered as one of the major pests of fresh tomatoes around the world. The species settled in north Africa in 2007, before being observed in the entire continent. Widespread insecticide use has led to the emergence of resistant populations in South America and Europe, but no large-scale insecticide resistance assessment has been performed in Sub-Saharan Africa so far. In this study, we collected T. absoluta larvae from locations widely distributed in Burkina Faso, where the pest was first detected in 2016. Acute toxicity of the all available molecules in Burkina Faso was evaluated in the laboratory on F1 individuals, including acetamiprid, abamectin, spinosad, cypermethrin, chlorpyrifos, λ-cyhalothrin, deltamethrin, and Bacillus thuringiensis. No LC50 differences among T. absoluta populations were highlighted, except for Bacillus thuringiensis. Insects were still highly susceptible to abamectin [LC50 < 0.4 mg/L; Control failure likelihood (CFL) = −25%], spinosad (LC50 < 0.6 mg/L; CFL = 25%) and chlorpyrifos-ethyl (LC50 between 254 and 458 mg/L; CFL = −15%), but were less susceptible to acetamiprid (CFL ranging from 72% to 91%), cypermethrin (CFL = 80%), λ-cyhalothrin (CFL =79%), and deltamethrin (CFL ranging from 51% to 66%), with LC50 values for these insecticides ranging between 100 and 525 mg/L. Pending a proper communication strategy, we hope this work could help producers avoiding the most inefficient active substances.     

Mutation in the ace‐1 gene of the tomato leaf miner (Tuta absoluta) associated with organophosphates resistance

The tomato leaf miner, Tuta absoluta (Lepidoptera: Gelechiidae), is a major invasive pest that has spread throughout many countries in the Mediterranean basin and parts of Asia over the last decade. The control of T. absoluta has relied heavily on the use of chemical insecticides, a strategy that has led to the evolution of resistance. In this study, biological and molecular methods were used to determine the susceptibility of five strains of T. absoluta to the organophosphate chlorpyrifos and to investigate the molecular mechanisms underlying resistance to this class of insecticides. High levels of resistance to chlorpyrifos were observed in all five strains tested. Cloning and sequencing of the gene encoding the organophosphate target site, ace‐1, of T. absoluta revealed the presence of an alanine to serine substitution at a position that has been previously linked with organophosphate resistance across a range of different insect and mite species. The presence of this mutation at high frequency in T. absoluta populations originating from various countries further supports the suggestion that the rapid expansion of this species is, in part, mediated by the resistance of this pest to chemical insecticides.     

Modeling the potential global distribution of light brown apple moth Epiphyas postvittana (Lepidoptera: Tortricidae) using CLIMEX

Light brown apple moth Epiphyas postvittana is a significant horticultural pest native to Australia that currently has a limited global distribution. However, this pest can tolerate very heterogeneous climates and has a wide host range. It has recently established in California with considerable consequences for US international and domestic trade. It has resulted in increasing calls for targeted risk assessment so that appropriate quarantine measures can be put in place to prevent its entry into new regions and further spread. Potential global distribution has been predicted by comparing the climatic conditions of its native (Australia) and long-established (New Zealand) ranges to the rest of the world using CLIMEX. It was suggested that E. postvittana has potential to establish mainly in countries in Central and South America, southern Africa, Western Europe and Southeast Asia. The study provides basic information for further assessment of the establishment capacity of this species in new habitats, and adds to the knowledge required to make science-based decisions in biosecurity.     

A multi‐genome analysis approach enables tracking of the invasion of a single Russian wheat aphid (Diuraphis noxia) clone throughout the New World

This study investigated the population genetics, demographic history and pathway of invasion of the Russian wheat aphid (RWA) from its native range in Central Asia, the Middle East and Europe to South Africa and the Americas. We screened microsatellite markers, mitochondrial DNA and endosymbiont genes in 504 RWA clones from nineteen populations worldwide. Following pathway analyses of microsatellite and endosymbiont data, we postulate that Turkey and Syria were the most likely sources of invasion to Kenya and South Africa, respectively. Furthermore, we found that one clone transferred between South Africa and the Americas was most likely responsible for the New World invasion. Finally, endosymbiont DNA was found to be a high‐resolution population genetic marker, extremely useful for studies of invasion over a relatively short evolutionary history time frame. This study has provided valuable insights into the factors that may have facilitated the recent global invasion by this damaging pest.     

Role of larval host plant experience and solanaceous plant volatile emissions in Tuta absoluta (Lepidoptera: Gelechiidae) host finding behavior

The tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae), is considered to be a major pest that damages tomato (Solanum lycopersicum L; Solanaceae) crops in South American, European, and Mediterranean countries. This insect species is polyphagous (i.e., feeds on many types of food); hence, it could also develop on other cultivated host plants, principally solanaceous plants, such as potato (S. tuberosum L.; Solanaceae) and eggplant (S. melongena L.; Solanaceae). Therefore, we tested the hypothesis that host plant choice by adult T. absoluta is influenced by plant volatile organic compounds and larval host plant experience. One tomato cultivar (cv.) ‘Moneymaker’ and three potato cv. ‘Charlotte’ ‘Bintje,’ and ‘Nicola’ were tested. Using a flying tunnel, we observed that females reared on tomato preferred flying toward tomato and, to a lesser extent, potato cv. ‘Charlotte.’ These preferences might be explained by the high release of terpenes by these two plants. When conducting oviposition choice assays, we found no preference between tomato and potato in the number of eggs laid by females that had been previously reared on either host plant. This study indicates that the host finding behavior of T. absoluta is mediated by solanaceous volatiles, while oviposition behavior appears to depend on additional stimuli. These results provide baseline information for use in the development of new control strategies against T. absoluta using semiochemicals and plant breeding.