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Abstract and Figures

Cowpea (Vigna unguiculata Walp.) is the most economically important legume crop in arid regions of sub-Saharan Africa. Cowpea is grown primarily by subsistence farmers who consume the leaves, pods and grain on farm or sell grain in local markets. Processed cowpea foods such as akara (a deep-fat fried fritter) are popular in the rapidly expanding urban areas. Demand far exceeds production due, in part, to a variety of insect pests including, in particular, the lepidopteran legume pod borer (LPB) Maruca vitrata. Genetically engineered Bt-cowpea, based on cry1Ab (Event 709) and cry2Ab transgenes, is being developed for use in sub-Saharan Africa to address losses from the LBP. Before environmental release of transgenic cowpeas, the Bt Cry proteins they express need to be assessed for potential effects on non-target organisms, particularly arthropods. Presented here is an assessment of the potential effects of those Cry proteins expressed in cowpea for control of LPB. Based on the history of safe use of Bt proteins, as well as the fauna associated with cultivated and wild cowpea in sub-Saharan Africa results indicate negligible effects on non-target organisms.
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Vol.:(0123456789)
1 3
Journal of Pest Science (2018) 91:1165–1179
https://doi.org/10.1007/s10340-018-0974-0
REVIEW
An assessment oftherisk ofBt‑cowpea tonon‑target organisms
inWest Africa
MalickN.Ba1· JosephE.Huesing2· ManueleTamò3· ThomasJ.V.Higgins4· BarryR.Pittendrigh5· LarryL.Murdock6
Received: 21 April 2017 / Revised: 15 March 2018 / Accepted: 16 March 2018 / Published online: 10 April 2018
© Springer-Verlag GmbH Germany, part of Springer Nature 2018
Abstract
Cowpea (Vigna unguiculata Walp.) is the most economically important legume crop in arid regions of sub-Saharan Africa.
Cowpea is grown primarily by subsistence farmers who consume the leaves, pods and grain on farm or sell grain in local
markets. Processed cowpea foods such as akara (a deep-fat fried fritter) are popular in the rapidly expanding urban areas.
Demand far exceeds production due, in part, to a variety of insect pests including, in particular, the lepidopteran legume pod
borer (LPB) Maruca vitrata. Genetically engineered Bt-cowpea, based on cry1Ab (Event 709) and cry2Ab transgenes, is
being developed for use in sub-Saharan Africa to address losses from the LBP. Before environmental release of transgenic
cowpeas, the Bt Cry proteins they express need to be assessed for potential effects on non-target organisms, particularly
arthropods. Presented here is an assessment of the potential effects of those Cry proteins expressed in cowpea for control
of LPB. Based on the history of safe use of Bt proteins, as well as the fauna associated with cultivated and wild cowpea in
sub-Saharan Africa results indicate negligible effects on non-target organisms.
Keywords Cowpea· Maruca vitrata· Bt-cowpea· Non-target organisms· West Africa· Environmental risk· Assessment·
Arthropod fauna
Key messages
Data on the environmental safety of Bacillus thuringien-
sis (Bt) Cry proteins, especially toward non-target arthro-
pods, are available for many genetically modified crops
but not in the contest of cowpea.
Before environmental release of Bt-cowpea for control of
the legume pod borer, a major insect pest attacking cow-
pea, the potential effects on non-target organisms (NTO),
particularly arthropods, need to be assessed.
An assessment of the Bt Cry proteins, their history of safe
use, as well as the fauna associated with cultivated and
wild cowpea in sub-Saharan Africa indicates negligible
effects on non-target organisms.
Introduction
Cowpea (Vigna unguiculata Walp.) is the most economically
important legume crop in West Africa (Langyintuo etal.
2003). Nigeria, Niger and nations surrounding these two
countries are the most productive cowpea lands globally,
Communicated by N. Desneux.
* Barry R. Pittendrigh
pittendr@msu.edu
1 International Crops Research Institute fortheSemi-Arid
Tropics, Niamey, Niger
2 United States Agency forInternational Development
(USAID), Washington, DC, USA
3 International Institute ofTropical Agriculture, Cotonou,
Benin
4 Commonwealth Scientific andIndustrial Research
Organisation (CSIRO), Agriculture andFood, Canberra,
Australia
5 Department ofEntomology, Michigan State University,
EastLansing, MI, USA
6 Department ofEntomology, Purdue University,
WestLafayette, IN, USA
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... There seems to be a general lack of empirical risk assessment studies. A more recent Bt cowpea study [61], which was compiled by experts who had already contributed to [59], does not mention any empirical testing of non-target organisms that are specific to Nigeria. ...
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We analyze the application filed for the marketing and cultivation of genetically engineered Bt cowpea (event AAT 709A) approved in Nigeria in 2019. Cowpea (Vigna ungiguiculata) is extensively grown throughout sub-Saharan Africa and consumed by around two hundred million people. The transgenic plants produce an insecticidal, recombinant Bt toxin meant to protect the plants against the larvae of Maruca vitrata, which feed on the plants and are also known as pod borer. Our analysis of the application reveals issues of concern regarding the safety of the Bt toxins produced in the plants. These concerns include stability of gene expression, impact on soil organisms, effects on non-target species and food safety. In addition, we show deficiencies in the risk assessment of potential gene flow and uncontrolled spread of the transgenes and cultivated varieties as well as the maintenance of seed collections. As far as information is publicly available, we analyze the application by referring to established standards of GMO risk assessment. We take the provisions of the Cartagena Protocol on Biosafety (CPB) into account, of which both Nigeria and the EU are parties. We also refer to the EU standards for GMO risk assessment, which are complementary to the provisions of the CPB.
... Plant-incorporated protectants (PIPs) are biopesticides such as the gene encoding the Bt toxin that can be introduced into the plant genome that allows the plant to produce this toxin and increases the resistance of the plant to some pests [178]. For instance, the Cry proteins expressed in Bt cowpeas have shown a less negative effect on nontarget organisms [179]. Generally, the PIPs available globally for the specific management of M. vitrata and A. fabae are limited, and equally, their impacts on their natural enemies have not been studied; thus, more work has to be done to address this gap. ...
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Common bean (Phaseolus vulgaris) production and storage are limited by numerous constraints. Insect pests are often the most destructive. However, resource-constrained smallholders in sub-Saharan Africa (SSA) often do little to manage pests. Where farmers do use a control strategy, it typically relies on chemical pesticides, which have adverse effects on the wildlife, crop pollinators, natural enemies, mammals, and the development of resistance by pests. Nature-based solutions —in particular, using biological control agents with sustainable approaches that include biopesticides, resistant varieties, and cultural tools—are alternatives to chemical control. However, significant barriers to their adoption in SSA include a lack of field data and knowledge on the natural enemies of pests, safety, efficacy, the spectrum of activities, the availability and costs of biopesticides, the lack of sources of resistance for different cultivars, and spatial and temporal inconsistencies for cultural methods. Here, we critically review the control options for bean pests, particularly the black bean aphid (Aphis fabae) and pod borers (Maruca vitrata). We identified natural pest regulation as the option with the greatest potential for this farming system. We recommend that farmers adapt to using biological control due to its compatibility with other sustainable approaches, such as cultural tools, resistant varieties, and biopesticides for effective management, especially in SSA.
... There are no unique arthropod (insect) species in the likely deployment area for Bt cowpea in Africa that have not been assessed elsewhere for other GM crops (Ba et al., 2018), so the existing data on the environmental safety of Cry1Ab to non-target organisms were sufficient to complete the environmental risk assessment of 709A cowpea. ...
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Published in Open Access Government (https://www.openaccessgovernment.org/major-insect-pests/111590/): Jose M. Barrero, Donald J. MacKenzie, Richard E. Goodman and T.J.V. Higgins provide an in-depth look at what we need to know about a biotech shield for cowpea against the major insect pests
... Currently, many researchers have focused a lot of effort into improving yields and increasing the production of crops [7,[11][12][13]. Cowpea (Vigna unguiculata L. Walp.) is an extensively cultivated plant, widely used as a legume in native tropical and subtropical zones or the semi-arid regions of South Africa [14]. Vigna unguiculata in rural areas (known as "Macunde beans") is a source of green manure, organic matter [15] for hay, forage and silage [16]. ...
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The aim of this study was to evaluate the adaptability of different genotypes of cowpea (Vigna unguiculata L. Walp.) in the edaphoclimatic conditions of a semi-arid region. In the experimental design, a completely randomized split-plot (2 × 8), with 3 repetitions (blocks) was used. The experiment comprised 7 new genotypes and 1 local genotype as the first main factor and application of insecticide as a secondary factor. Two-factor analysis of variance (two-way ANOVA) determined the differences between the treated and untreated plots. The results obtained in the experiment showed that the introduced genotypes V3 (IT07K-181-55), V7 (H4), and V5 (IT97K-556-4M) adapted well to the edaphoclimatic conditions of the study area and their yields were respectively 1019, 1015, and 841 kg/ha of grains in treated plots and 278, 517 and 383 kg/ha in untreated plots. Multivariate analysis revealed that the most important parameter was the germination rate. Finally, the best yield was obtained with the genotype V3 (IT07K-181-55), subjected to the use of insecticide, and with the V7 (H4) genotype in untreated plants. The findings presented in this research should be useful in crop system agricultural programs, particularly in the terms of selection of cultivating systems suitable for high-yielding cowpea.
... In Egypt, cowpea is promising double purpose forage and seed crop for its green canopy or using it in animal diets as dry seeds, as well as it is a primary source of plant protein for humans and animals in the summer season (HamdAlla et al., 2014). It is the most economically important legume crop in arid regions of sub-Saharan Africa (Ba et al., 2018). However, Singh and Allen (1979) reported that major insect pests of cowpea that cause economic losses are cowpea aphids (Aphis craccivora Koch), leafhoppers (Empoasca spp.), thrips (Megalurothrips sjostedti Trybom), flower-feeding beetles (Mylabris spp. ...
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The present investigation was carried out at Giza Agricultural Experiments and Research Station, Agricultural Research Center (ARC), Giza, Egypt during the two successive seasons 2016 and 2017. The objective of this investigation was to assess the effect of applied irrigation water, infestation with insects and infection with virus on cowpea and maize productivity, as well as farmer income under intercropping condition. The experiment included nine treatments which were the combinations between three applied irrigation water levels (80, 100 and 120% of the recommended applied irrigation water level of maize) and three cropping systems (intercropping cowpea with maize, sole cowpea and sole maize), in addition to recommended sole maize that grown on ridges 70 cm width and received 100% of applied irrigation water. The experimental design was a strip plot with three replications. Irrigation water treatments were randomly assigned to the vertical strips and cropping systems were allocated in the horizental strips. Data indicated that the highest applied irrigation water level (120% ETo) had higher water consumptive use than the others. The intercrops had higher water consumptive use than those of sole plantings. With respect to maize crop, increasing applied irrigation water from 80 to 120% ETo significantly increased infestation with ap hids, jassids, Hawaiian beet webworm, cotton leafworm and whiteflies on maize leaves, as well as higher grain yield per ha and its attributes. Intercropped maize had higher infestatio n with aphids, jassids, cotton leafworm and whiteflies, as well as ear leaf area per plant than those of sole maize, meanwhile, the reverse was true for greater sugarcane borer. Intercropped maize plants that received the highest applied irrigation water (120% ETo) had higher infestation with aphids, jassids and cotton leaf worm on maize leaves than the other treatments, meanwhile higher ear leaf area per plant was recorded by application of the recommended applied irrigation water of maize (100% ETo). With respect to cowpea crop, increasing applied irrigation water from 80 to 120% ETo significantly increased infestation with aphids, jassids, leaf miner fly, Hawaiian beet webworm, cotton leafworm and whiteflies, as well as soybean mosaic virus (SMV) infection on cowpea leaves, beside higher plant height, number of branches per plant and forage yield per ha. Intercropped cowpea had lower infestation with aphids, jassids, leaf miner fly and Hawaiian beet webworm, as well as lower SMV infection and number of branches per pla nt and forage yield per ha than those of sole cowpea. Sole cowpea that received the recommended applied irrigation water of maize (100% ETo) had higher infestation with Hawaiian beet webworm, jassids and leaf miner fly on cowpea leaves than the other treatments, meanwhile, SMV infection was not by the interaction b etween applied irrigation water levels and cropping systems. Sole cowpea that received the highest applied irrigation water level (120% ETo) had a higher number of branches per plant and fora ge yield per ha than the other treatments. With respect to compet itive and water relationships, as well as economic return, land equivalent ratio (LER) and land equivalent coefficient (LEC) gave higher values over 1.00 and 0.25, respectively, with higher water equivalent ratio (WER) and net return by intercropping cowpea with maize that received 100% ETo in both seasons. These results show that growing two rows of maize on beds 140 cm width (one row/side) with growing two rows of cowpea in middle of maize beds with the application of the recommended applied irrigation water level of maize reduced aphids, jassids and cotton leafworm on maize leaves, and jassids, leaf miner fly and Hawaiian beet webworm on cowpea leaves, as well as increased maize grain and cowpea forage yields per ha, land and water usages, as well as econ omic return.
... Recently, a pod borer resistant Bt cry1Ab cowpea event AAT709A has been approved for release in Nigeria (Addae et al. 2020). The biosafety assessment of Bt cowpea has revealed negligible effects on non-target organisms (Ba et al. 2018). Bt cowpea will reduce the damage caused by MPB which may result in increase in crop yield, reduce pesticide usage, and improve environment and farmers' health and their income. ...
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Key message Fertile independent transgenic cowpea lines expressing the BtCry2Aa toxin with increased resistance to the most devastating lepidopteran insect pest, Maruca pod borer has been developed for the first time. Abstract Cowpea is a staple legume important for food and nutritional security in sub-Saharan Africa and Asia, where its production is limited by the key pest, legume pod borer (Maruca vitrata). Cowpea varieties resistant to M. vitrata are not known, hence, development of Maruca pod borer resistance cowpea through genetic engineering is a promising approach to improve its production. In the present study, transgenic cowpea plants expressing Bacillus thuringiensis Cry2Aa insecticidal protein were developed for the first time using Agrobacterium tumefaciens-mediated transformation of cotyledonary explants. T0 plants recovered from Agrobacterium cocultured explants on medium containing 120 mgl⁻¹ of kanamycin were identified on the basis of the presence of transgenes by PCR, their integration into genome by Southern hybridization and expression of their transcripts by semi quantitative PCR (sqRT-PCR) and quantitative Real–time-PCR (qRT-PCR) and protein by Western blot analysis. The transformation efficiency obtained was 3.47% with 11 independent T0 transgenic lines. The bioefficacy of Cry2Aa protein expressed in randomly selected four T0 plant’s leaves and pods was evaluated by feeding Maruca pod borer demonstrated a significant lower damage and a high level of Maruca mortality (more than 90%) for all these Bt lines. The inheritance of transgenes from T0 to T1 progeny plants was demonstrated by PCR analysis. The transgenic plants generated in this study can be used in cowpea breeding program for durable and sustainable legume pod borer resistance.
... Cowpea has been transformed with the cry1Ab gene construct from B. thuringiensis, which was highly toxic to M. vitrata (94). The development of transgenic cowpea was accompanied by complementary studies targeting its environmental (48) and non-target organism risk assessment (11), as well as by insect resistance management (87). Since Bt-cowpea with a single gene would inevitably lead to resistance in M. vitrata, the possibility of stacking the vegetative insecticidal protein (vip) gene from B. thuringiensis with a dissimilar mode of action than cry1Ab was assessed (14). ...
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Full text can be accessed at the following URL: http://www.annualreviews.org/eprint/MVAQH6RACZFWNYSKSD98/full/10.1146/annurev-ento-021220-084539 ********************************************************* Legume pod borer, Maruca vitrata, has emerged as a major pest on food legumes in Asia and Africa. It is an oligophagous pest, feeding on over 70 species in Fabaceae. We examine the species complex in Asia, Africa, Oceania, and the Americas, with an emphasis on molecular taxonomy. Studies on pheromone production and perception suggest the existence of pheromone polymorphism, especially in Asia and Africa. No Maruca-resistant varieties are available in the major food legumes including cowpea, pigeonpea, mungbean, and yard-long bean. Legume growers use chemical pesticides indiscriminately, leading to the development of pesticide resistance. However recent developments in habitat management, classical biocontrol with more efficient parasitoids, biopesticides, and judicious use of insecticides pave the way for sustainable management of M. vitrata, which can reduce the pesticide misuse. Active engagement of the private sector and policy makers can increase the adoption of integrated pest management approaches in food legumes.
... In Egypt, cowpea is promising double purpose forage and seed crop for its green canopy or using it in animal diets as dry seeds, as well as it is a primary source of plant protein for humans and animals in the summer season (HamdAlla et al., 2014). It is the most economically important legume crop in arid regions of sub-Saharan Africa (Ba et al., 2018). However, Singh and Allen (1979) reported that major insect pests of cowpea that cause economic losses are cowpea aphids (Aphis craccivora Koch), leafhoppers (Empoasca spp.), thrips (Megalurothrips sjostedti Trybom), flower-feeding beetles (Mylabris spp. ...
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The present investigation was carried out at Giza Agricultural Experiments and Research Station, Agricultural Research Center (ARC), Giza, Egypt during the two successive seasons 2016 and 2017. The objective of this investigation was to assess the effect of applied irrigation water, infestation with insects and infection with virus on cowpea and maize productivity, as well as farmer income under intercropping condition. The experiment included nine treatments which were the combinations between three applied irrigation water levels (80, 100 and 120% of the recommended applied irrigation water level of maize) and three cropping systems (intercropping cowpea with maize, sole cowpea and sole maize), in addition to recommended sole maize that grown on ridges 70 cm width and received 100% of applied irrigation water. The experimental design was a strip plot with three replications. Irrigation water treatments were randomly assigned to the vertical strips and cropping systems were allocated in the horizental strips. Data indicated that the highest applied irrigation water level (120% ETo) had higher water consumptive use than the others. The intercrops had higher water consumptive use than those of sole plantings. With respect to maize crop, increasing applied irrigation water from 80 to 120% ETo significantly increased infestation with aphids, jassids, Hawaiian beet webworm, cotton leafworm and whiteflies on maize leaves, as well as higher grain yield per ha and its attributes. Intercropped maize had higher infestation with aphids, jassids, cotton leafworm and whiteflies, as well as ear leaf area per plant than those of sole maize, meanwhile, the reverse was true for greater sugarcane borer. Intercropped maize plants that received the highest applied irrigation water (120% ETo) had higher infestation with aphids, jassids and cotton leafworm on maize leaves than the other treatments, meanwhile higher ear leaf area per plant was recorded by application of the recommended applied irrigation water of maize (100% ETo). With respect to cowpea crop, increasing applied irrigation water from 80 to 120% ETo significantly increased infestation with aphids, jassids, leaf miner fly, Hawaiian beet webworm, cotton leafworm and whiteflies, as well as soybean mosaic virus (SMV) infection on cowpea leaves, beside higher plant height, number of branches per plant and forage yield per ha. Intercropped cowpea had lower infestation with aphids, jassids, leaf miner fly and Hawaiian beet webworm, as well as lower SMV infection and number of branches per plant and forage yield per ha than those of sole cowpea. Sole cowpea that received the recommended applied irrigation water of maize (100% ETo) had higher infestation with Hawaiian beet webworm, jassids and leaf miner fly on cowpea leaves than the other treatments, meanwhile, SMV infection was not by the interaction between applied irrigation water levels and cropping systems. Sole cowpea that received the highest applied irrigation water level (120% ETo) had a higher number of branches per plant and forage yield per ha than the other treatments. With respect to competitive and water relationships, as well as economic return, land equivalent ratio (LER) and land equivalent coefficient (LEC) gave higher values over 1.00 and 0.25, respectively, with higher water equivalent ratio (WER) and net return by intercropping cowpea with maize that received 100% ETo in both seasons. These results show that growing two rows of maize on beds 140 cm width (one row/side) with growing two rows of cowpea in middle of maize beds with the application of the recommended applied irrigation water level of maize reduced aphids, jassids and cotton leafworm on maize leaves, and jassids, leaf miner fly and Hawaiian beet webworm on cowpea leaves, as well as increased maize grain and cowpea forage yields per ha, land and water usages, as well as economic return.
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