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Biocontrol of Pests of Apples and Pears in Northern and Central Europe: 1. Microbial Agents and Nematodes

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The viral, bacterial, fungal and nematode pathogens of arthropod pests of apple and pear in northern and central Europe and their use as biocontrol agents are reviewed. Baculoviruses are important viral pathogens of several lepidopterous pests of apple and pear but other viral pathogens have not been investigated in depth and are little known. The granuloviruses of codling moth, Cydia pomonella (CpGV), and to a lesser extent, of the summer fruit tortrix moth, Adoxophyes orana (AoGV), have been researched extensively and are exploited as biological control agents. Commercial development and use has been limited because of their high costs, slow action, short persistence and specificity relative to broad-spectrum pesticides. The widespread development of strains of codling moth multi-resistant to insecticides and the desire to reduce dependence on pesticides have improved the commercial prospects of CpGV and use is likely to increase. The development of a genetically improved egt-strain of CpGV (lacking the ecdysteroid-UDP glucosyl transferase gene) in the UK is a significant breakthrough, though commercialization in the UK may be difficult due to adverse public attitudes to the release of genetically-modified microorganisms. Future research and development approaches include further genetic manipulation of CpGV and AoGV to improve potency, speed of kill and/or persistence, improvement of formulation (to reduce UV light sensitivity) and development of cheaper mass production techniques and possibly in vitro production. A systematic search for baculoviruses and other viruses of apple and pear pests is likely to reveal important new opportunities. The most important bacterial pathogen used as a biological control agent is Bacillus thuringiensis (Bt). However, Bt products currently available have limited effectiveness against many orchard pests due to the pests' cryptic life habits. The HD-1 Bt strain has been investigated and used extensively for control of leaf-rolling tortricid larvae and is widely used, but efficacy is moderate. Advances in biotechnology and genetic engineering provide opportunity for development of Bt strains designed specifically to control orchard pests, but this has not yet been done for commercial reasons. Other research approaches include the evaluation of new Bt products developed for other markets worldwide and the bioassay of strains from Bt collections against specific apple or pear pests. Entomopathogenic fungi provide good opportunity for development as biological control agents of apple and pear pests. The main factor limiting their effectiveness is the requirement for high humidities and moderate temperatures for spore germination and development. For foliar pests, a useful starting point for research might be the control of sucking pests which excrete honeydew (e.g. Cacopsylla sp. or aphids) or those that inhabit protected microenvironments (e.g. Dasineura sp.). Key areas for research are improved formulation, the selection of low temperature-active strains, field evaluation and avoiding possible adverse effects of fungicides. An alternative approach is to examine the exploitation of entomopathogenic fungi in soil, to which many species of entomopathogenic fungi are adapted ecologically. Apple and pear orchards provide long-term stable habitats where populations of entomopathogenic fungi in soil are likely to be large. There are few important soil pests of apple or pear. However, many species spend part of their life in soil, mainly to pupate or overwinter, where they may be targeted by fungal entomopathogenic biocontrol agents. Entomopathogenic nematodes have many attributes which favour them as biological control agents. However, their requirement for surface moisture for survival and movement means there are only limited prospects for using them as biological control agents for foliar pests. As with entomopathogenic fungi, there are better prospects for control of pests that occur in soil. Microbial pathogens and entomopathogenic nematodes are important components of the natural enemy complex of apple and pear orchards and more effort needs to be devoted to fostering them and exploiting them as biocontrol agents in sustainable, biologically-based Integrated Pest Management programmes. They can in many cases be mass produced at low cost by bulk fermentation processes and applied as sprays (as 'biopesticides') and are, at least potentially, ideal biological control agents for many apple or pear pests. Important general characteristics are their comparative environmental and human safety, compatibility with other control strategies in Integrated Pest Management programmes and reproductive capacity. They tend to be effective in a narrower range of environmental conditions than pesticides, but there is considerable potential to improve their effectiveness by improved formulation, strain selection and genetic manipulation. They are often host-specific and thus, offer restricted marketing opportunities, which is a significant barrier to development and commercialisation. Registration procedures and associated fees for microbial agents are a further significant barrier. Such requirements do not apply currently to nematodes.
... For example, studies of insect pests of apple orchards in the Rhône valley in France do not mention A. crataegi (Simon et al. 2011); nor does a review of integrated crop management and organic systems for apple production in Europe as a whole (Tresnik & Parente 2007). There is no mention, either, of A. crataegi in three companion papers on the control of pests of apples and pears in northern and central Europe (Cross et al. 1999a(Cross et al. , 1999bSolomon et al. 2000), or in a more recent study of the control of invertebrate pests of pears across Europe (Shaw, Nagy & Fountain 2021). Nor could we find any recent mention of the butterfly as a pest of cultivated Prunus, cherries or plums (e.g., Jaastad et al. 2004;Quero-García et al. 2017). ...
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The black-veined white butterfly, Aporia crataegi, reached the north-western edge of its European geographic distribution in the British Isles in the 19th century, but became extinct in the early 20th century, following several cold decades. Substantial areas of potential breeding habitat in southern Britain are currently available to this species, which requires scattered hawthorn (Crataegus monogyna) and suckering blackthorn scrub (Prunus spinosa), including infrequently cut hedgerows. These habitats are needed at a relatively large scale as the butterfly occurs as networks of colonies (metapopulations), ranging over large tracts of connected landscape. A number of events have increased habitat availability over the past 70 years (myxomatosis reduced rabbit populations, which permitted host plant scrub regeneration; hedgerow management policies reduced cutting frequencies; rewilding and landscape connectivity initiatives are resulting in additional scrub). However, while A. crataegi males occasionally disperse several kilometres, it is unlikely that A. crataegi females will cross the English Channel in sufficient numbers to establish populations in southern England, without assistance. Here, we (i) provide a review of the literature on species interactions, the habitat requirements, distribution and dispersal of A. crataegi and (ii) provide evidence that southern, eastern and central England are likely to be climatically suitable for reintroductions of A. crataegi. Substantial areas of England are already expected to be amongst the climatically most suitable parts of Europe for this insect. We identify a landscape of at least 100 km2 containing multiple patches of suitable habitats, and highlight co-benefits for other species that inhabit scrubland and successional mosaics. We use a climate-matching approach to assess climatically-similar locations to obtain source material most likely to establish in Britain. Areas of northern France and mid elevations in the Iberian Peninsula, including in the Pyrenees, provide potential suitable source locations due to close climatic matching and a large number of species records. We recommend reestablishment from more than one source, providing genetic diversity in the reintroduced population, enabling subsequent local adaptation to British conditions. We highlight the opportunity for monitored releases to be undertaken within the landscape highlighted here, so as to evaluate population growth, host plant use, and rates of colonisation away from release sites that differ in their management, habitat, host plant characteristics, and proximity to other sites. This approach would aim to develop knowledge as a living lab to inform future best practice releases. In conclusion, the black-veined white, A. crataegi, has potential to become a model species for assisted colonisation projects where natural and human-created barriers have prevented range expansion into regions where the 21st century climate is suitable for a species.
... Biological control has long been implemented against C. pomonella, which includes entomopathogenic fungi, viruses, nematodes, bacteria, and microsporidia [40]. The betabaculovirus Cydia pomonella granulovirus (CpGV) is a highly efficacious and selective virus, which has been produced as a commercial product in Europe and North America and utilised globally for the control of C. pomonella since the early 1990s [41,42]. Two commercial products, Carpovirusine ® (Arysta LifeScience, Noguères, France) and Madex ® (Andermatt-Biocontrol AG, Grossdietwil, Switzerland), both of which are formulated with the Mexican CpGV isolate, are utilised in South Africa for the control of C. pomonella [43]. ...
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Baculovirology has been studied on the African continent for the development of insect virus-based biopesticides and, to a much lesser extent, vaccine production and delivery, since the 1960s. In this review, we focus only on baculoviruses as biopesticides for agricultural pests in Africa. At least 11 species of baculovirus have been discovered or studied on the African continent, some with several distinct isolates, with the objective in most cases being the development of a biopesticide. These include the nucleopolyhedroviruses of Helicoverpa armigera, Cryptophlebia peltastica, Spodoptera exempta, Spodoptera frugiperda, Spodoptera littoralis, and Maruca vitrata, as well as the granuloviruses of Cydia pomonella, Plutella xylostella, Thaumatotibia (Cryptophlebia) leucotreta, Choristoneura occidentalis, and Phthorimaea operculella. Eleven different baculovirus-based biopesticides are recorded as being registered and commercially available on the African continent. Baculoviruses are recorded to have been isolated, researched, utilised in field trials, and/or commercially deployed as biopesticides in at least 13 different African countries. Baculovirus research is ongoing in Africa, and researchers are confident that further novel species and isolates will be discovered, to the benefit of environmentally responsible agricultural pest management, not only in Africa but also elsewhere.
... The development of resistance against chemical insecticides by pests such as WAA, as well as concerns regarding the deleterious effects of chemicals on the environment, have provided a strong drive for the development of microbial agents to be used in controlling insect pests (Inglis et al. 2001). Entomopathogenic fungi (EPF) have the potential to be used for biological control of sap-sucking insects such as the WAA, which cannot easily be controlled using chemical pesticides and other biological control means (Chandler et al. 1997;Wraight et al. 1998;Cross et al. 1999a;Pu et al. 2005). The potential of EPF for biological control was first noticed during the 19th century by Metchnikoff, in 1879, and by Krassilstschik, in 1888, when they mass-produced Metarhizium anisopliae (Metchn.) ...
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Eriosoma lanigerum (Hausmann) (Hemiptera: Aphididae), woolly apple aphid (WAA) is an important pest on apples globally and a key pest of apple production in South Africa. The aphid has developed some level of resistance against several chemical insecticides. Entomopathogenic fungi (EPF) have been identified as promising biological control agents against a wide array of insect pests. The main aim of this study was to conduct a survey in local apple orchards in the Western Cape province for EPF and to use isolates to test the susceptibility of WAA under optimum laboratory conditions. Soil samples were collected from apple orchards and EPF, baited and isolated using larvae of Galleria mellonella and Tenebrio molitor. Six EPF species: Beauveria bassiana, Cordyceps fumosorosea, Metarhizium brunneum, M. pinghaense, M. robertsii and Purpureocillium lilacinum were identified from the soil samples. The results from bioassays showed that Metarhizium robertsii and M. pinghaense isolates were the most effective with an average percentage mortality of > 90%. Metarhizium brunneum also proved to be effective when used against the insect with an average percentage mortality of > 80%, while B. bassiana and C. fumosorosea were the least effective with average percentage mortality of 52% and 48%, respectively. The LT50 and LT90 of M. robertsii (2.12; 4.19) and M. pinghaense (2.05; 4.45) showed to require similar mortality time in days of E. lanigerum. The results obtained in the study have provided an insight into the diversity of EPF species across apple orchards of the Western Cape and shown the efficacy of the Metarhizium isolates as potential biological control agents of the WAA.
... The development of resistance against chemical insecticides by pests such as WAA, as well as concerns regarding the deleterious effects of chemicals on the environment, have provided a strong drive for the development of microbial agents to be used in controlling insect pests (Inglis et al. 2001). Entomopathogenic fungi (EPF) have the potential to be used for biological control of sap-sucking insects such as the WAA, which cannot easily be controlled using chemical pesticides and other biological control means (Chandler et al. 1997;Wraight et al. 1998;Cross et al. 1999a;Pu et al. 2005). The potential of EPF for biological control was first noticed during the 19th century by Metchnikoff, in 1879, and by Krassilstschik, in 1888, when they mass-produced Metarhizium anisopliae (Metchn.) ...
Article
Full-text available
Eriosoma lanigerum (Hausmann) (Hemiptera: Aphididae), woolly apple aphid (WAA) is an important pest on apples globally and a key pest of apple production in South Africa. The aphid has developed some level of resistance against several chemical insecticides. Entomopathogenic fungi (EPF) have been identified as promising biological control agents against a wide array of insect pests. The main aim of this study was to conduct a survey in local apple orchards in the Western Cape province for EPF and to use isolates to test the susceptibility of WAA under optimum laboratory conditions. Soil samples were collected from apple orchards and baited using larvae of Galleria mellonella and Tenebrio molitor to isolate EPF. Six EPF species: Beauveria bassiana, Cordyceps fumosorosea, Metarhizium brunneum, M. pinghaense, M. robertsii and Purpureocillium lilacinum were identified from the soil samples. The results from bioassays showed that Metarhizium robertsii and M. pinghaense isolates were the most effective with an average percentage mortality of > 90%. Metarhizium brunneum also proved to be effective when used against the insect with an average percentage mortality of > 80%, while B. bassiana and C. fumosorosea were the least effective with average percentage mortality of 52% and 48%, respectively. The lethal time required to kill 50% and 90% of the colony at a concentration of 107 conidia/ml over five days, LT50 and LT90, of M. robertsii (2.12 and 4.19 days, respectively) and M. pinghaense (2.05 and 4.45 days, respectively) showed to require similar mortality time in days of E. lanigerum. The results obtained in the study have provided an insight into the diversity of EPF species across apple orchards of the Western Cape and shown the efficacy of the Metarhizium isolates as potential biological control agents of the E. lanigerum.
... The use of bacteria as biocontrol agents and plant growth promoters is not a novel concept and has been reported in a number of scholarly articles from around the world (Oostendorp et al., 1991;Cross et al., 1999;Khan and Kim, 2007;Timper, 2014;Xiang et al., 2018;Dutta et al., 2019). Several bacterial genera, including Bacillus, Pseudomonas, Arthrobacter, Burkholderia, Pasteuria, Achromobacter, Rhizobium, and Serratia, have been identified as nematicidal. ...
... Leaf litter, fruit and vegetable bins, bark, pruning wounds, and nutshells are included in cryptic habitats. Many researchers have documented the effective control of insects residing in cryptic habitats (Lacey and Shapiro-Ilan 2008;Cross et al. 1999;Lacey et al. 2007;Shapiro-Ilan et al. 2005). EPNs successfully controlled the worldwide distributed insect pest of apple and pome fruit, i.e., codling moth (Cydia pomonella) in cryptic habitat. ...
Chapter
Entomopathogenic fungi are microorganisms capable of infecting and killing arthropods and therefore have a great potential in pest management. As the extensive use of synthetic pesticides has led to increased resistance in insects, decreased natural enemies, and had negative impacts on environmental and human health, the search for eco-friendly control agents is urgent. Entomopathogenic fungi are promising alternatives in this regard and are attracting global attention, with increasing efforts and financial investments being made for the development, commercialization and use of fungus-based control products. Despite scientific and technological advances, there is still a need for studies to expand the number of species applicable in pest management and improve their performance in the field. There is also a need to increase user awareness regarding their correct use with the aim to establish their widespread adoption and market potential. This chapter covers the main taxonomic groups that comprise entomopathogenic fungi, their modes of action to establish insect infection and spread, and the insect’s defense mechanisms against these fungi. Furthermore, techniques of fungal isolation, selection, and production are discussed. The usage status, challenges, and prospects of mycoinsecticides are also addressed, highlighting their application potential for sustainable agricultural production.
... Leaf litter, fruit and vegetable bins, bark, pruning wounds, and nutshells are included in cryptic habitats. Many researchers have documented the effective control of insects residing in cryptic habitats (Lacey and Shapiro-Ilan 2008;Cross et al. 1999;Lacey et al. 2007;Shapiro-Ilan et al. 2005). EPNs successfully controlled the worldwide distributed insect pest of apple and pome fruit, i.e., codling moth (Cydia pomonella) in cryptic habitat. ...
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Biopesticides, using living microbial bodies and their bio-active composites against insects, are potential replacements for synthetic insecticides for safer and modern food production systems. Entomopathogenic bacteria (EPB) are important biological control agents of insect pests since the last century. Though bacterial species have been documented to be used against insects for developing symbiotic relationships, only a few of them are identified as entomopathogens. Most of these are members of the family Bacillaceae, Enterobacteriaceae, Pseudomonadaceae, Clostridiaceae, and Neisseriaceae. More than 100 bacterial species have been reported to infect various arthropods. Bacillus thuringiensis (Bt), B. sphaericus, B. cereus, and B. popilliae are the most appreciated microbial pest control agents. However, new bacterial species also need to be explored for their entomopathogenic role and materialized as new biopesticide products. The commercial biopesticides based on novel EPBs with improved genetic materials must be a part of future research for effective integrated pest management programs. This present chapter highlights the classification, infection, replication, transmission mechanisms, and important EPB in integrated pest management.
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This bibliometric review provides a comprehensive analysis of the evolving landscape of biopesticide research within the realm of fruit crop protection. Recognizing the increasing global demand for sustainable agricultural practices, we undertook a systematic examination of the scientific literature to uncover key trends, influential authors, prolific journals, and emerging themes in biopesticide applications for fruit crops. Our analysis spans a defined timeframe, revealing the trajectory of research efforts and their impact on sustainable fruit production. The review highlights the growing importance of biopesticides as eco-friendly alternatives to conventional chemical pesticides, shedding light on the dynamic interplay between biological control agents and fruit pests. Moreover, we identify gaps in current knowledge and propose avenues for future research to address challenges in the widespread adoption of biopesticides. This bibliometric exploration serves as a valuable resource for researchers, policymakers, and practitioners seeking a deeper understanding of the current state and future directions of biopesticide research in the context of fruit agriculture.
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Thesis
p>The effect of surface material on the electrostatic charge of house-flies ( Musca domestica) was investigated. It was found that the charge of M. domestica is dependent on the material upon which they walk. Charge is gained through triboelectrification, the exchange of electrons with a surface through contact and friction. Charge level was found to be a function of distance moved though each different surface material elicits a different maximum charge on M. domestica. This maximum charge is reached after approximately 30 cm. Two methods were developed for measuring the electrical charge of insects. The first involved placing individuals into a Faraday pail, which is calibrated to measure the net charge of objects that are contained within. In the second method, individual M. domestica were connected directly to an electrostatic voltmeter. Electrical charge was found to be proportional to the non-contact pick-up of dielectric particles from a surface by an in vitro M. domestica wing. Experiments with live flies indicated that the charge gained from triboelectrification on a surface affects the pick-up of particles. This could have important implications in the choice of construction material for an autoinoculation trap for the dissemination of entomopathogens. The conidiospores of the entomopathogenic fungus Metarhizium anisopliae were formulated with carnauba wax particles. Carnuaba wax is a strong dielectric and can carry a strong electrostatic charge. Formulation with carnauba wax in a 1:5 ratio was found to conserve conidia in a simulated bait station without significantly affecting mortality. Such formulation also reduces the loss of conidia from inoculated flies to the environment. Because less conidia are lost to the environment, indirect transmission from inoculated flies to the environment to uninfected individuals is reduced, however, this is not seen as an important process in the autodissemination of fungal entomopathogens. Conidia formulated with wax are transmitted horizontally in cage conditions, from fly to fly, but less readily than unformulated conidia.</p
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In 1994, a survey of pheromone trap catches of adult males of 11 species of tortricid moths known to feed on apple in the larval stage was done in 10 apple orchards in England. The orchards were of three broadly different types with differing histories of insecticide management. One sex pheromone trap for each of the 11 species surveyed viz Adoxophyes orana, Archips podana, A. rosana, Ditula angustiorana, Epiphyas postvittiana, Pandemis ceresana, P. heperana, Ptychloma lecheana, Hedya dimidioalba, Spilonota ocellana, Cydia pomonella was placed in each orchard in May 1994 and the number of moths of the target species, and of incidentals, was recorded at 2-3 week intervals until October 1994. A blank trap, with no pheromone lure was also included in each orchard. The codling moth, C. pomonella, was most numerous in the cider orchards (with >500 moths caught per trap), followed by the unsprayed orchards and least numerous in the intensively sprayed commercial Cox orchards. The reverse was true for A. orana which, within its established geographic range, was most numerous in intensively treated Cox orchards. It occurred in sprayed and unsprayed orchards in Oxfordshire, the first record of this species in the county. It was absent from the cider orchards in the west and south west. A. podana occurred in moderate numbers (with 100-300 moths per trap) in all orchards. P heperana, hitherto not regarded as a significant pest in Britain, was caught in low to moderate numbers in all orchards. It was most numerous in the unsprayed desert and culinary apple orchards. Variable numbers (2 to 308 per trap) of H. dimidioalba were also caught. There was no relationship between insecticide management and numbers caught. The pest status of H. dimidioalba and P heperana in Britain requires further investigation. Small but variable catches of P. lecheana, S. ocellana and P. ceresana occurred at most sites. Catches of A. rosana, and D. angustiorana were zero or very low throughout. E. postvittana, was absent from all the orchards surveyed. In addition to the target species, each pheromone lure type attracted at least one and usually several other non- target species of Lepidoptera as incidentals. Those which were frequently recorded had common or similar pheromone components to the target species, or in some cases with other incidentals captured in the same trap. This implies that the pheromone components of some species are incorrectly or incompletely known.
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These largely non-specific parasites come into contact with tortricoids only when the mature larva searches for a diapausing or pupation site in or near the soil. The discussion is divided into mermithid and steinernematid nematodes, considering their classification and bionomics, as well as some host-parasite relationships, and lastly the use of Neoaplectana carpocapsae in the biological control of codling moth. -J.W.Cooper