sfs-03b-2014 eu-china cooperation on ipm in...

of 13

This project has received funding from the European Union’s Seventh Framework Programme for research, technological development and demonstration under the Grant Agreement n°613817

Copyright © 2014, MODEXTREME Consortium

Horizon 2020 Programme

SFS-03b-2014 EU-China cooperation on IPM in agriculture

EU-CHINA Lever for IPM Demonstration

Project ID: 633999

Deliverable number : D2.1

Deliverable title : Feasibility study on SIT-based approaches for management of key pests

EC version : V1

Due date of deliverable 30/09/2017 (M24)

Actual submission date 19/01/2018 (M29)

Ref. Ares(2018)334330 - 19/01/2018

DOCUMENT INFO

1. Author(s)

Organisation name lead contractor INRA

Author Organisation e-mail Adam WALKER Oxitec [email protected]

2. Revision history

Version Date Modified by Comments 1

3. Dissemination level

PU Public

CO Confidential, only for members of the consortium (excluding the Commission Services)

EUCLID - Europe-China Lever for IPM Demonstration [email protected] - www.euclidipm.org

EXECUTIVE SUMMARY

Background

In response to growing concerns associated with the use of insecticides for crop protection - such as insect resistance, off-target effects to the ecosystem and risks to human health - regulations are being imposed to restrict their use. As a consequence, growers are seeking more environmentally preferable insect control alternatives which reduce dependence on conventional insecticides and increasingly following an Integrated Pest Management (IPM) approach.

Objectives and methods

Oxitec’s self-limiting control technology uses advanced genetics to offer an alternative insect control strategy, that is insect-specific, and can augment existing IPM strategies. The feasibility of applying Oxitec’s technology to a given pest however, is reliant on a variety of technical, economic, social, and regulatory aspects. Here, we discuss the feasibility of applying Oxitec’s insect control approach to five important pest insects of tomato, grape, and cruciferous vegetables.

Results & implications

Our findings raise some important points for further investigation before developing a self-limiting control strategy for any of these pest insects.


Table of contents

Introduction ............................................................................................................................................................................. 5

1. Oxitec control technology ......................................................................................................................................... 5

1.1. Male-selecting technology ......................................................................................................... 5

2. Insect pests selected for this feasibility study .................................................................................................. 6

2.1. Tuta absoluta (tomato leaf miner); ............................................................................................. 6

2.2. Lobesia botrana (grape berry moth) .......................................................................................... 6

2.3. Eupoecilia ambiguella (vine moth) ............................................................................................. 6

2.4. Plutella xylostella (diamondback moth) ...................................................................................... 6

2.5. Delia radicum (cabbage root fly) ................................................................................................ 6

3. Potential for laboratory mass-rearing ................................................................................................................. 7

4. Information required about the biology of the wild insect.......................................................................... 7

4.1. Do they reproduce sexually? ..................................................................................................... 7

4.2. Will the released insects be harmful to the crop? ...................................................................... 8

4.3. How far can the insect disperse? ............................................................................................... 8

4.4. How many insect generations are there in a control season? .................................................... 8

4.5. Do different populations of the insect exist and do mating barriers occur between them? ......... 8

5. Compatibility of the self-limiting approach with IPM.................................................................................... 9

6. Economic justification ................................................................................................................................................ 9

5.1. Pest impact in the target area despite existing control practices ...............................................10

5.2. Expected treatment area size ...................................................................................................10

5.3. Monitoring pest population dynamics........................................................................................10

5.4. Logistics associated with mass rearing .....................................................................................10

7. Concluding remarks ................................................................................................................................................. 11

References ............................................................................................................................................................................. 11


Introduction

Pest insects cause significant economic damage to agriculture throughout the world. The Food and Agriculture Organization (FAO) reports that a fifth of the world’s crop production is destroyed by insects annually [1] with damage caused by feeding, the introduction of plant pathogens, or infestation of stored products. In 2016, the estimated economic losses in crop and forest production due to invasive insect species amounted to a minimum of US$3.6 billion per year in Europe [2], whilst in China, they exceeded US$18.9 billion [3] and in the United States, were almost US$40 billion per year [4]. Pest control has traditionally involved insecticide use [5]; however, many insecticides are now ineffective or have been found to be harmful to people or the environment. In much of the world, intensive insecticide use has led to development of resistance to the majority of chemical classes [6] and the removal of natural enemies, which can enable further proliferation of resistant pests [7]. There are also other off-target effects. Pollinator decline has been associated with insecticide use and aerial spraying can cause insecticides to drift from the target site into wildlife areas [8]. In response to these issues, international legislations have been implemented to regulate insecticide usage. In the EU, a directive specifies that Member States adopt National Action Plans to reduce risks and impacts of pesticides and to encourage the development and introduction of alternative approaches such as IPM, to reduce dependence on insecticides [9]. Oxitec’s insect technology offers an alternative pest management approach which can complement existing methods. It involves releasing genetically engineered, ‘self-limiting’ males of a given pest insect to mate with wild females and pass on a self-limiting genetic trait which prevents survival of their offspring. Releases of self-limiting insects can eliminate pest populations that are inaccessible to traditional control methods, reducing the requirement for insecticides and any associated toxic residues in the environment. In addition, only the target pest insect species is directly affected, leaving beneficial insects unaffected [10]. Oxitec’s genetic control approaches have the potential to be used to control a variety of pest species, but feasibility of this is dependent on a number of factors. These include: the potential to mass-rear and genetically transform the target insect, the field biology of the pest, compatibility of current/future integrated pest management (IPM) methods, and economic justification. The following report discusses the feasibility of applying two of Oxitec’s approaches against key pests of tomato, grape and leafy vegetables, taking technical, biological, and economic aspects into consideration.

1. Oxitec control technology

1.1. Male-selecting technology

Here, the pest insect is engineered to express a male-selecting genetic trait. In the mass-rearing facility, this enables production of male-only adults for release and in the field, mating between released males and wild females prevents female offspring from surviving to reproductive age. Pest control is achieved by overflooding rates of male releases over a period of time which reduces the number of females in, and consequently the reproductive potential of, the wild pest population (population suppression) [11]. The technique also offers an insecticide resistance management benefit to complement IPM programs, which is discussed later. Self-limiting insects also carry a genetic marker to enable field monitoring during a control programme [12].


2. Insect pests selected for this feasibility study

2.1. Tuta absoluta (tomato leaf miner);

Originating from South America, T. absoluta now threatens solanaceous crops throughout the world. Tomatoes are primarily targeted, but other cultivated crops infested include aubergine, potato, sweet pepper and tobacco. Damage is caused by the larvae mining plant leaves, stems and aerial fruits and can reach 100% yield losses in some cases. Insecticides are traditionally used to control T. absoluta, however limited success has been experienced due to the cryptic nature of the larvae and the development of resistance to a variety of chemical classes. New IPM strategies include pheromones for lure and kill and mating disruption, natural enemies, Bacillus thuringiensis (Bt)-based insecticide formulations, host plant resistance and various cultural practices [13].

2.2. Lobesia botrana (grape berry moth)

A grape pest and serious threat to all vine-growing areas. Crop damage is primarily caused by the larvae feeding on the flower buds and fruits, however indirect damage is generally more devastating, as larvae feeding on grapes introduce pathogens such as fungal rots which reduce wine quality [14]. Chemicals are the most broadly used control strategy, due to their high efficiency and low cost, though insecticide resistance has been reported [15]. IPM is now the recommended strategy and includes techniques such as, phytosanitary control, cultural control, (Bt)-based insecticide formulations, natural enemies and mating disruption [14].

2.3. Eupoecilia ambiguella (vine moth)

Along with L. botrana, E. ambiguella is considered the most important insect pest of European vineyards. Larvae damage flowers, immature berries, and parts of the seed through direct feeding and secondary infections. E. ambiguella is listed as a harmful organism in a number of continents and is considered a threat to the grape industry in the United States if it were to become established [16]. Control can include a variety of techniques, such as insecticides, mating disruption [17, 18] and biological control [19].

2.4. Plutella xylostella (diamondback moth)

Considered to be the main insect pest of cruciferous vegetables worldwide, crops targeted include cabbages, broccoli, cauliflowers, canola and mustard. In 2012, it was estimated to cost the world economy US$4-5 billion annually through production costs and losses [20]. Having been the first insect reported to be resistant to Dichlorodiphenyltrichloroethane (DDT) and subsequently (Bt), P. xylostella has developed resistance to almost every insecticide applied in the field. The current trend is to develop and implement insecticide resistance management (IRM) programmes to conserve efficacy of viable insecticides. Due to control failures and pressure to reduce insecticide use in agriculture, alternative approaches are sought. Some to have shown promise include trap cropping, adult trapping, and pheromone disruption [21].

2.5. Delia radicum (cabbage root fly)

One of the major pests of commercially produced cruciferous crops in North America and Europe [22]. Crop targets include cabbages, broccoli, cauliflowers, Brussels sprouts, horseradish, swede and radish. Larvae eat the lateral roots and then bore into the tap root, and sometimes the base of the stem, causing stunted plant growth and death [23]. In Newfoundland, it is the single most important economic pest of vegetables [24]. Adequate control of D. radicum, particularly of the second generation, is a challenge, also the number of insecticides available for D. radicum control has steadily decreased and continues to decline [24]. Present control options include between-row inter-plantings [25], entomopathogenic fungi, nematodes, natural enemies [26], netting around plants, sticky traps and crop rotation to stop larvae populations from building up in the soil [27].


3. Potential for laboratory mass-rearing

In order to develop Oxitec’s control technology for a new species, it is crucial that the target species can be artificially reared in the laboratory. This is because genetically engineered strains which are generated to express a self-limiting trait are dependent on an additive which permits their survival in the laboratory or factory, but not in the field [28]. It is much easier to regulate the additive level that the insect receives via an artificial feeding system than a host plant. To establish a new insect in the laboratory, the availability of an existing laboratory-reared colony is preferable, as it reduces the time otherwise spent adapting the wild insect to a sustainable artificial diet, developing efficient rearing systems and developing techniques essential for germline transformation. If such a colony is unavailable, published artificial diets and rearing systems can be a useful alternative. To evaluate the feasibility of laboratory mass-rearing the pest insects selected for this analysis, a literature search of laboratory-reared colonies and published protocols was conducted. The findings are summarised in the table below: Table 1. Existing laboratory-reared colonies and artificial feeding systems for selected insects

Species Laboratory-reared colony Artificial feeding system

T. absoluta Yes [29] Yes [29]

L. botrana Yes [30] Yes [30, 31]

E. ambiguella Yes [31] Yes [32]

P. xylostella A laboratory-reared colony is already available at Oxitec Yes

D. radicum Yes [33] None found

Findings here offer promise for laboratory mass-rearing the selected insects and generating self-limiting strains. In most cases, both a laboratory-reared colony and protocols for artificial feeding systems were identified. The exception was D. radicum, for which only a laboratory-reared colony was found, however artificial diets for other brassica pests exist, such as Delia brassicae [34], which could be tested and/or modified to rear this insect. Our literature search also has positive implications for collective rearing the selected insects, as we could find no evidence for regular cannibalism in any of the insect species, which would reduce time and labour. We also found a published technique for collecting and handling eggs for all insects, which is an important part of insect germline transformation. Looking further ahead, Oxitec’s control strategies rely on the released males mating a high proportion of wild females in the target population to reduce the reproductive potential below a sustainable threshold. An effective insect mass-rearing system is essential for this, so our findings of published laboratory-reared colonies and artificial feeding systems for selected insects offers promise to develop economic programme scale mass rearing.

4. Information required about the biology of the wild insect

Various aspects of a pest insect’s biology in the field will determine if it is a suitable target for a self-limiting control programme. The following section discusses the main considerations, with reference to the insects included in this analysis.

4.1. Do they reproduce sexually?

Oxitec’s control techniques depend on the released males mating with wild females to pass the self-limiting genetic trait to their offspring, therefore species that reproduce asexually would be unsuitable targets [35]. A review of the literature found that all insects included in this study, with the exception of T.absoluta, only reproduce sexually. The occurance of asexual reproduction in T. absoluta [36] potentially has important implications for the effectiveness of a self-limiting control program against this pest. Before developing self-limiting strains of T. absoluta, a study of the potential target population would be necessary to find out whether asexual reproduction occurs and how frequently, to determine if the self-limting control technique is a suitable option.


4.2. Will the released insects be harmful to the crop?

Despite the long-term benefits that self-limiting insects provide by suppressing wild pest populations, releases of large numbers of insects that may cause transient damage could complicate growers’ acceptance of a control program [37]. A literature review of all insects in this study, found that only the larval stages cause crop damage, suggesting that adult or pupal releases would be suitable.

4.3. How far can the insect disperse?

The dispersal capacity of a pest species can determine the need to isolate treatment areas from immigration and is the primary factor dictating a population-wide approach [38]. A review of the literature found that most of the selected insects usuaully disperse less than 3km during their lifetime [39, 40, 41, 42, 43], so long-distance immigration of wild insects should not be problematic for a control programme. Furthermore, the impact of short distance immigration might not be either, depending on the programme goals. For example, if only moderate suppression is required to reduce crop damage beneath a threshold, small amounts of wild immigration may be tolerated [38]. Advantageously, when T. absoluta occurs on glasshouse cultivated tomatoes, wild immigration may not even be an issue at all, because in this circumstance the target population is already isolated. Moreover, the dispersal distances reported for all insects suggest that if release points are appropriately spaced, released males should be able to mix throughout the target population, avoiding the occurrence of isolated pools of wild insects from which internal re-infestations could occur. Importantly, if any self-limiting insects were to disperse outside of the target area, the genetic trait is not able to persist in field populations of the pest.

4.4. How many insect generations are there in a control season?

The amount of time it takes for a management programme to have a noticeable impact is dependent in part on the generation time of the target species, whereby a shorter generation time is preferable [37]. However, slow development in the field could be advantageous, as the pest population is unlikely to reach a very high level over the course of the season. From the perspective of developing self-limiting strains by recombinant DNA methods, insects with a shorter generation time typically make the process quicker [37]. A literature review found that the longest generation time was reported for D. radicum in northern climates, where only one generation can be completed in a growing season, however this increases to 2 or 3 in the warmer middle belt of Europe [44]. In contrast, the shortest generation time was reported for P. xylostella, where 10-14 generations have been recorded in the tropics [21]. If planning a self-limiting control programme for any of these pest insects, it would be critical to know the lifecycle of the target population to determine the timing and frequency of male releases. For example, to control D. radicum in northern climates, accurately predicting the single emergence of wild adults would be crucial to ensure that male releases coincide with this. If this were impractical, the technique may be more effective on populations in warmer climates and other control options preferable in cooler climates. In contrast, to control P. xylostella in the tropics, frequent year-round releases of males would be necessary to prevent wild population explosions - a mass-rearing facility would need to be able to cope with these insect production demands. From the perspective of strain development, findings from this literature review have positive implications for all of these insects as warmer temperature was found to reduce generation time. This suggests that increasing the temperature at which the insects are reared could accelerate the process required to develop transgenic strains.

4.5. Do different populations of the insect exist and do mating barriers occur between them?

If the target species are multiple species, or different populations with strong premating barriers between them, then rearing and releasing only one type may be of limited benefit [37]. A literature review only found evidence of a mating barrier in L. botrana, whereby allopatric populations occur that show non-random mating [45]. In D. radicum, sympatric populations were found to exist, but there was no evidence of a mating barrier, only timing of adult emergence [46] - further research on the mating compatibility within target populations of D. radicum would be necessary to determine if a mating barrier exists. However to control L. botrana, selecting the correct population to mass rear and release would be crucial. This section has primarily focussed on the biology of the wild insect, however when preparing for a self-limiting control programme, there are several other technical aspects concerning the mass reared males which would warrant investigation. Of major importance is that released males can compete well enough with the wild males to


successfully mate and inseminate the targeted wild females. Performance metrics such as dispersal, longevity, location of mating arenas, courtship, mating, and sperm transfer would therefore need assessment [47]. When male performance is understood from this perspective, the effectiveness of a self-limiting approach for a specific insect can be better determined.

5. Compatibility of the self-limiting approach with IPM

The principle of IPM is to take advantage of all appropriate pest management strategies and integrate them in a way that protects crops with the least possible disruption to agro-ecosystems [48]. This involves keeping insecticides and other interventions at economically acceptable levels to encourage beneficial species such as natural enemies and pollinators, whilst minimizing risks to human health and the environment [49]. The self-limiting control technology is a pest management strategy suited to IPM. The approach targets a single species, so it can dramatically reduce the environmental impact of insect control, particularly in comparison to conventional insecticides which can harm many other species including beneficial insects. Although it could be used as a standalone method, it works efficiently and economically when pest populations have already been reduced by other control strategies [37]. A reason for this is that treatment area size is determined by the number of self-limiting males that can be mass produced. If there are fewer wild insects in the treatment area because of other interventions, then a larger area can be treated, or a higher release ratio can be achieved in the original area [50]. Moreover, any insect control technique that reduces the population density either before or during the application of a self-limiting control program can improve its own efficiency. For example, the use of biocontrol organisms is generally most effective at high pest densities, but loses efficiency as pest densities decrease. A self-limiting control program can work very efficiently at low pest densities and therefore complements biocontrol, in the same way it would other strategies, such as insecticides and pheromonal mating disruption [50]. All of the insects under evaluation here are controlled using these strategies and others, so the self-limiting insect control technique could be included in an existing IPM programme, or a new one, so long as other criteria, such as regulatory and political acceptance, are met. Essentially, the self-limiting technique will combine effectively with any other method which does not specifically target self-limiting males over wild ones [37]. The male-selecting approach also offers an insecticide resistance management benefit. Mating between released males and wild females results in the survival of male hemizygotes for the genetic trait and the introgression of their genetic background into the wild pest population. If the released males have an insecticide-susceptible genetic background, then this insecticide susceptibility will increase in the population as the wild population gets diminished [51]. A suggested application is the management of Bt crop resistance, as a number of insect populations have developed resistance to this strategy. A male-selecting approach could restore the effectiveness of Bt crops in affected areas, whilst preventing further resistance developing. This would also benefit other control programs where insecticides have been the only effective control method available. Resistance management relies on the release of susceptible males, so it would be necessary to maintain insecticide susceptibility during mass rearing processes, prior to release. The same would apply where insects have developed resistance to sprayed applications of the bio-insecticide Bt. Ultimately, the best strategy for controlling any of the selected insects most likely involves a combination of several methods. Therefore, the optimal strategy is likely to be an IPM program which includes a self-limiting component when suitable [37].

6. Economic justification

The feasibility of a self-limiting control approach against a given pest, cannot be determined by a technical evaluation alone, an economic justification must also be performed [52]. For the Sterile Insect Technique (SIT), a benefit/cost


analysis (BCA) is applied, whereby the overall value of the technique against alternative insect management options are compared over a specified period of time – the same approach can be applied to a self-limiting control programme. This section discusses some important points from a BCA checklist [52] with respect to a self-limiting control programme and selected insects. Ultimately though, a detailed BCA would be performed for the specific pest in the proposed treatment area [52].

5.1. Pest impact in the target area despite existing control practices

If the control techniques presently used are ineffective, this could be a significant incentive for a self-limiting control programme [52]. Despite current control practices, all of the selected insects are reported to cause significant economic damage to their respective hosts throughout the world [13, 14, 16, 20, 23]. Insecticides are the most commonly used control strategy, however in many examples this approach has been unsuccessful due to factors such as insect resistance, cryptic behaviour [13], and regulations on use. With an increasing international preference for IPM strategies which reduce insecticide residues, a self-limiting approach would be a suitable option. Also, as previously described, the technique could improve the efficiency of other control strategies to further increase crop value, due to its effectiveness at low pest densities [50]. However, to justify including a self-limiting approach, information on current crop losses over several seasons in the target area, would also be helpful [52].

5.2. Expected treatment area size

The size of the treatable area is largely influenced by the goal of the programme. If the goal is to eradicate the pest from a treatment area and protect it from reinvasion, a larger release zone would be required. However, if the goal is to suppress the pest, whereby a certain damage threshold is tolerated, relatively smaller release zones and protective buffers would be adequate [53]. The size of the treatable area using a self-limiting control programme is largely influenced by the capacity to mass rear insects and the logistics associated with releases [52]. However, when used in combination with other pest management strategies which initially reduce the target population, the treatable area could be extended without increasing rearing costs [50]. In the case of T. absoluta, glasshouse horticulture offers an ideal arena for self-limiting control. It is enclosed, so there would be minimal immigration and emigration, plus the crop is extremely high value so a preventative measure would be a highly attractive strategy.

5.3. Monitoring pest population dynamics

A substantial amount of the budget for a self-limiting control programme will be designated to insect monitoring, to gain information about population dynamics pre-release, evaluate progress during the programme and confirm the status of control during the post-release phase [52]. A substantial benefit of self-limting insects is that they carry a genetic marker to aid field monitoring. This avoids the need to add dyes to the artificial feeding system and can reduce or eliminate the number of false positive insects caught on monitoring traps - which is especially important when a programme is in the eradication phase. They also offer a robust backup option, whereby PCR genotyping can be used to confirm the identity of insects caught on monitoring traps [54].

5.4. Logistics associated with mass rearing

One of the key requirements for the success of the technique is the production of sufficient insects, in sufficient number and of adequate quality. Since a self-limiting control programme would compete economically with other control techniques, insect production must be timely and cost-effective [52]. Generally, small insects with rapid life cycles are cheap to rear whereas those which require individual containment, or specialized environments can affect mass production costs [52]. Larval cannibalism is an example where individual containment would be required [38]. A literature review found that larval cannibalism was not common amongst the selected insects and only tends to occur in response to overcrowding. When large numbers of insects are required for a self-limiting control programme, it is possible to take advantage of economies of scale in the rearing facility. For example, ingredients used in artificial feeding systems, other innovations and automation could be optimised for cost effectiveness. In addition, a major advantage of the male-selecting technology is the ability to remove large numbers of females simultaneously, by witholding a dietary additive. Male-only production reduces the amount of diet required by the pre-release generation and improves the mating efficiency of released males with wild females. This section has highlighted some of the key points to consider from a BCA checklist, however in practice, for a given treatment area, the analysis would be approached through a series of steps [52]. A timescale that accounts for all phases of a control programme would need defining. In addition, various technical and economic aspects would be


required to determine the geographic scale. Costs associated with control, and other management activities would need to be determined. Finally, benefits should be measured through such factors as, current costs and losses in the area to be controlled, the development of additional market opportunities, and the reduction of pesticide applications and residues [52].

7. Concluding remarks

This feasibility study has raised some important points for further investigation from a technical, biological and economic viewpoint, concerning each of the selected pest insects. However, the decision to implement a self-limiting control programme does not just depend on these viewpoints. Ultimately, all approaches that use releases of genetically engineered insects will require regulatory and public acceptance. This would be dependent on a variety of factors, including laws and regulations of the country where a control programme is intended, along with various social, environmental, and political considerations. However, given increasing trends towards effective control strategies which can reduce the negative impacts of insecticide use - such as insect resistance, various off target effects and harm caused to human health and the environment - the self-limiting control technology should be considered an advantageous option.

References

1. INSECT DAMAGE: Damage on Post-harvest. “Introduction”. INSECT DAMAGE Post-harvest Operations.

fao.org, 2000. Web. 2000.

2. Bradshaw C. J. A., Leroy B., Bellard C., Roiz D., Albert C., Fournier A., Barbet-Massin M., Salles J-M., Simard

F., Courchamp F. 2016. Massive yet grossly underestimated global costs of invasive insects. Nature

Communications.

3. Wan F. H., Yang N. W. 2015. Invasion and Management of Agricultural Alien Insects in China. Annual Review

of Entomology 61: 77-98.

4. Paini D., Sheppard A., Cook D., De Barro P., Worner S., Thomas M. 2016. Global threat to agriculture from

invasive species.

5. Pimentel D., Krummel J., Gallahan D., Hough J., Merrill A., Schreiner I., Vittum P., Koziol F., Back E., Yen D.,

Fiance S. 1978. Benefits and Costs of Pesticide Use in U.S. Food Production. BioScience 28: 772–784.

6. Denholm I., Cahill M., Dennehy T. J., Horowitz A. R. 1998. Challenges with managing insecticide resistance in

agricultural pests, exemplified by the whitefly Bemisia tabaci.” Philosophical Transactions of the Royal Society

B: Biological Sciences 353.1376: 1757–1767.

7. Luck R. F., Van den Bosch R., Garcia R. 1977. Chemical Insect Control—A Troubled Pest BioScience 27:

606–611.

8. Wells M. Vanishng bees threaten US crops. “Pesticides?”. news.bbc.co.uk, 2007. Web. Mar. 11th 2007.

9. Directive 2009/128/ec of the european parliament and of the council of 21 October 2009. "Establishing a

framework for Community action to achieve the sustainable use of pesticides". Legal content. EUR-lex, 2009.

Web. Nov. 24th of 2009.

10. Developing GM Insect Technologies. “The Potential Benefits of GM Insect Strategies”. Genetically Modified

Insects. inasp.info, 2010. Web. Jun. 2010.

11. Jin L., Walker A., Fu G., Harvey-Samuel T., Dafa’alla T., Miles A., Marubbi T., Granville D., Humphrey-Jones

N., O’Connell S., Morrison N., Alphey L. 2013. Engineered Female-Specific Lethality for Control of Pest

Lepidoptera. ACS Synthetic Biology: 160-166.

12. Fraser MJ Jr. 2012. Insect transgenesis: current applications and future prospects. Annual Review of

Entomology 57:267-289.


13. Desneux N., Wajnberg E., Wyckhuys K., Burgio G., Arpaia S., Narváez-Vasquez C., González-Cabrera J.,

Catalán Ruescas D., Tabone E., Frandon J., Pizzol J., Poncet C., Cabello T., Urbaneja A. 2010. Biological

invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for

biological control. Journal of Pest Science 83: pp 197–215.

14. Lobesia botrana (grape berry moth). Invasive Species Compendium. cabi.org, 2017. Web. 2017

15. Civolani S., Boselli M., Butturini A., Chicca M., Fano E., Cassanelli S. 2014. Assessment of Insecticide

Resistance of Lobesia botrana (Lepidoptera: Tortricidae) in Emilia-Romagna Region. Journal of Economic

Entomology 107: 1245–1249.

16. Damage. “Grape”. Eupoecilia ambiguella. USDA-APHIS-PPQ-CPHST, 2014. Web. Nov. 2014.

17. Louis F., Schirra K. 2001. Mating disruption of Lobesia botrana (Lepidoptera: Tortricidae) in vineyards with very

high population densities. Pheromones for Insect Control in Orchards and Vineyards IOBC wprs Bulletin 24:

75-79.

18. Arn H., Louis F. 1997. Mating Disruption in European Vineyards. Insect Pheromone Research: 377-382.

19. Omkar. 2016. Mating Disruption as a Component of Integrated Pest Management. Ecofriendly Pest

Management for Food Security 1st Edition; 579 – 580.

20. Zalucki M., Shabbir A., Silva R., Adamson D., Liu S., Furlong M. 2012. Estimating the Economic Cost of One of

the World's Major Insect Pests, Plutella xylostella (Lepidoptera: Plutellidae): Just How Long Is a Piece of

String? Journal of economic entomology: 1115 – 1129.

21. Plutella xylostella (diamondback moth). Invasive Species Compendium. cabi.org, 2014. Web. Dec. 9th of 2014.

22. Santolamazza-Carbone s., Velasco P., Cartea M. E. 2017. Resistance to the cabbage root fly, Delia radicum

(Diptera, Anthomyiidae), of turnip varieties (Brassica rapa subsp. rapa). Euphytica: 213 - 274.

23. cabbage root fly (Delia radicum). “Symptoms”. Plantwise Knowledge Bank. plantwise.org, 2017. Web. 2017.

24. Dixon, P. L., Coady, J. R., Larson, D. J. and Spaner, D. 2004. “Undersowing rutabaga with white clover: impact

on Delia radicum (Diptera: Anthomyiidae) and its natural enemies,” The Canadian Entomologist: 427–442.

25. Concepts and Directions in Arthropod Pest Management. “Cultural Management”. Delia radicum.

sciencedirect.com, 2017. Web. 2017.

26. Finch, S. Integrated pest management of the cabbage root fly and the carrot fly. 1993. Crop Protection 12: 423-

430.

27. Cabbage root fly Delia radicum. “Treatment”. Pests and diseases. bbc.co.uk, 2014. Web. 2014.

28. Thomas, D., Donnelly, C., Wood, R., Alphey, L. 2000. Insect Population Control Using a Dominant,

Repressible, Lethal Genetic System. Science: 2474-2476.

29. Bajonero, J., Parra, J. 2017. Selection and Suitability of an Artificial Diet for Tuta absoluta (Lepidoptera:

Gelechiidae) Based on Physical and Chemical Characteristics. Journal of Insect Science 17: 13.

30. Moreau, J., Monceau, K., Thiéry, D. 2015. Larval food influences temporal oviposition and egg quality traits in

females of Lobesia botrana. Journal of Pest Science 89: 439–448.

31. Tzanakakis, M., Savopoulou, M. 1973. Artificial Diets for Larvae of Lobesia botrana (Lepidoptera: Tortricidae).

Annals of the Entomological Society of America 66: 470 – 471.

32. Thiéry, D., Moreau, J. 2005. Relative performance of European grapevine moth (Lobesia botrana) on grapes

and other hosts. Oecologia 143: 548-557.

33. Shuhang, W., Voorrips, R., Steenhuis-Broers, G., Vosman, B., van Loon, J. 2016. Antibiosis resistance against

larval cabbage root fly, Delia radicum, in wild Brassica-species. Euphytica 211: 139–155.

34. Singh, P. 1977. Artificial Diets for Insects, Mites, and Spiders.

35. Alphey, L., Alphey, N. 2014. Five Things to Know about Genetically Modified (GM) Insects for Vector Control.

PLoS Pathog 10(3.

36. Megido, R., Haubruge, E., Verheggen, F. 2012. First evidence of deuterotokous parthenogenesis in the tomato

leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Journal of Pest Science 85: 409–412.

37. Alphey, L., Benedict, M., Bellini, R., Clark, G., Dame, D., Service, M., Dobson, S. 2010. Sterile-Insect Methods

for Control of Mosquito-Borne Diseases: An Analysis. Vector Borne Zoonotic Diseases 10: 295-311.

38. Lance, D., McInnis, D. 2005. Biological Basis of the Sterile Insect Technique. Sterile Insect Technique: 69 – 87.

39. Salama, H., Abdel-Khalek, I., Fouda, M., Ebadah, I., Shehata, I. 2015. Some Ecological and Behavioral

Aspects of the Tomato Leaf Miner Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). ECOLOGIA

BALKANICA 7: 35-44.

40. Saour, G. 2016. Flight Ability and Dispersal of European Grapevine Moth Gamma-Irradiated Males

(Lepidoptera: Tortricidae). Florida Entomologist 99: 73-78.

41. Hardman, J. 2012. Modelling Arthropods to Support IPM in Vineyards. Arthropod Management in Vineyards:

37-52.


42. Shirai, Y., Nakamura, A. 1994. Dispersal Movement of Male Adults of the Diamondback Moth, Plutella

xylostella (Lepidoptera: Yponomeutidae), on Cruciferous Vegetable Fields, Studied Using the Mark-Recapture

Method. Applied Entomology and Zoology 29: 339-348.

43. Finch, S., Skinner, G. 1982. Upwind flight by the cabbage root fly, Delia radicum. Physiological Entomology 7;

387–399.

44. Pests. “Delia radicum (L.) - Root Fly, Spring Cabbage Fly, Radish Maggot”. Interactive Agricultural Ecological

Atlas of Russia and Neighbouring Countries. agroatlas.ru, 2003-2009. Web. 2003-2009.

45. Muller, K., Thiéry, D., Delbac, L. and Moreau, J. 2016. Mating patterns of the European grapevine

moth,Lobesia botrana(Lepidoptera: Tortricidae) in sympatric and allopatric populations. Biological Journal of

the Linnean Society.

46. Walgenbach, J., Eckenrode, l., Straub, R. 1993. Emergence Patterns of Delia radicum (Diptera: Anthomyiidae)

Populations from North Carolina and New York. Environmental Entomology Journal 22: 559-566.

47. Koyama, J., Kakinohana, H., Miyatake, T. 2004. Eradication of the melon fly, Bactrocera cucurbitae, in Japan:

importance of behavior, ecology, genetics, and evolution. Annual Review of Entomology 49: 331-349.

48. Introduction to Integrated Pest Management. “Principles of IPM”. United States Environmental Protection

Agency. epa.gov, 2017. Web. Aug. 18th of 2017.

49. AGP - Integrated Pest Management. “FAO definition”. Food and Agriculture Organisation of the United Nations.

fao.org, 2017. Web. 2017.

50. The Sterile Insect Release Method and Other Genetic Control Strategies. “Integration into Pest Management

Programs”. Radcliffe's IPM World Textbook. ipmworld, 2017. Web. 2017.

51. Harvey-Samuel, T., Morrison, N., Walker, A., Marubbi, T., Yao, J., Collins, H., Gorman, K., Davies, T., Alphey,

N., Warner, S., Shelton, A. and Alphey, L. (2015). Pest control and resistance management through release of

insects carrying a male-selecting transgene. BMC Biology.

52. Mumford, J. 2005. Application of Benefit/cost Analysis to Insect Pest Control Using the Sterile Insect

Technique. Sterile Insect Technique; 481-498.

53. Hendrichs, J., Vreysen, M., Enkerlin, W., Cayol, J. 2005. Strategic Options in Using Sterile Insects for Area-

wide Integrated Pest Management. Sterile Insect Technique; 564-596.

54. Walters, M., Morrison, N., Claus, J., Tang, G., Phillips, C., Young, R., Zink, R. and Alphey, L. 2012. Field

Longevity of a Fluorescent Protein Marker in an Engineered Strain of the Pink Bollworm, Pectinophora

gossypiella (Saunders). PLoS ONE.

sfs-03b-2014 eu-china cooperation on ipm in...

Documents