ArticlePublisher preview available

An assessment of the risk of Bt-cowpea to non-target organisms in West Africa

September 2018
Journal of Pest Science 91(8)

DOI:10.1007/s10340-018-0974-0

Projects: Insect Toxicology
Insect resistant chickpea

Authors:

Malick Ba

Consultative Group on International Agricultural Research

Joseph E. Huesing

United States Agency for International Development (USAID)

Manuele Tamo

Consultative Group on International Agricultural Research

T. J. V. Higgins

The Commonwealth Scientific and Industrial Research Organisation

Show all 6 authorsHide

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.

Web food table of herbivores that feed upon cowpea in West Africa (Adati et al. 2007; Bottenberg et al. 1998; Jackai and Daoust 1986; Singh and Allen 1980; Singh and Van Emden 1979; Dreyer 1994)

…

Figures - available from: Journal of Pest Science

This content is subject to copyright. Terms and conditions apply.

A preview of this full-text is provided by Springer Nature.
Learn more

Preview content only

Content available from Journal of Pest Science

This content is subject to copyright. Terms and conditions apply.

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

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.

Deficiencies in the Risk Assessment of Genetically Engineered Bt Cowpea Approved for Cultivation in Nigeria: A Critical Review

Article

Full-text available

Jan 2022

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.

Natural Pest Regulation and Its Compatibility with Other Crop Protection Practices in Smallholder Bean Farming Systems

Article

Full-text available

Aug 2021

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.

A biotech shield for cowpea against the major insect pests

Article

Full-text available

May 2021

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

Modeling of Cowpea (Vigna unguiculata) Yield and Control Insecticide Exposure in a Semi-Arid Region

Article

Full-text available

May 2021

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.

STUDY OF PRODUCTIVITY AND ECONOMIC EVALUATION OF INTERCROPPING COWPEA WITH MAIZE UNDER THREE IRRIGATION WATER LEVELS AND THEIR RESPONSE TO INSECT INFESTATION AND VIRAL INFECTION

Article

Full-text available

Jan 2021

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.

Transgenic cowpea plants expressing Bacillus thuringiensis Cry2Aa insecticidal protein imparts resistance to Maruca vitrata legume pod borer

Article

Full-text available

Mar 2021
PLANT CELL REP

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.

Emergence of Maruca vitrata as a Major Pest of Food Legumes and Evolution of Management Practices in Asia and Africa

Article

Jan 2021

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.

Study of productivity and economic evaluation of intercropping cowpea with maize under three irrigation water levels and their response to insect infestation and viral infection

Article

Full-text available

Jan 2021

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.

Developing Climate-Resilient Cowpea (Vigna unguiculata [L.]Walp.) Through Genomics-Assisted Breeding Approaches

Chapter

Jan 2022

Anticipating farmer outcomes of three genetically modified staple crops in sub-Saharan Africa: Insights from farming systems research

Article

Aug 2021
J RURAL STUD

Conventional ex-ante evaluations rely on a mix of economic, environmental, and social indicators to assess the potential impacts of Genetically Modified (GM) crops prior to their commercial release. While these predictive studies have produced useful knowledge, they have also consistently overestimated the ex-post outcomes of GM crops for African smallholder farmers. Yet these same assessment methods remain the dominant approach to project farmer outcomes for a new suite of soon-to-be commercialized GM staple crops. The research presented in this paper offers a different evaluative approach for these new GM crops by taking inspiration from farming systems research (FSR). We use the conceptual starting point of FSR scholarship—the farming system—to conduct an exploratory predictive analysis of three GM crops currently in the experimental pipeline: Water Efficient Maize for Africa (WEMA) in Kenya, disease-resistant matooke banana in Uganda, and Bt cowpea in Burkina Faso. Our findings suggest that the lofty projected benefits of these crops are unlikely to be realized by many, if not most, smallholder farmers due to incongruences with the farming systems they are designed to benefit. This research demonstrates the importance of using farming system-based evaluation methods to better anticipate likely farm-level outcomes of new breeding technologies.

Bt rice in China - focusing the non-target risk assessment

Article

Full-text available

Mar 2017
PLANT BIOTECHNOL J

Bt rice can control yield losses caused by lepidopteran pests but may also harm non-target species and reduce important ecosystem services. A comprehensive data set on herbivores, natural enemies, and their interactions in Chinese rice fields was compiled. This together with an analysis of the Cry protein content in arthropods collected from Bt rice in China indicated which non-target species are most exposed to the insecticidal protein and should be the focus of regulatory risk assessment. This article is protected by copyright. All rights reserved.

Biological control: a major component for the long-term cowpea pest management strategy

Article

Full-text available

Jan 2012

Silicone wristbands detect individuals’ pesticide exposures in West Africa

Article

Full-text available

Aug 2016

We detected between 2 and 10 pesticides per person with novel sampling devices worn by 35 participants who were actively engaged in farming in Diender, Senegal. Participants were recruited to wear silicone wristbands for each of two separate periods of up to 5 days. Pesticide exposure profiles were highly individualized with only limited associations with demographic data. Using a 63-pesticide dual-column gas chromatography–electron capture detector (GC-ECD) method, we detected pyrethoid insecticides most frequently, followed by organophosphate pesticides which have been linked to adverse health outcomes. This work provides the first report of individualized exposure profiles among smallholder farmers in West Africa, where logistical and practical constraints have prevented the use of more traditional approaches to exposure assessment in the past. The wristbands and associated analytical method enabled detection of a broad range of agricultural, domestic, legacy and current-use pesticides, including esfenvalerate, cypermethrin, lindane, DDT and chlorpyrifos. Participants reported the use of 13 pesticide active ingredients while wearing wristbands. All six of the pesticides that were both reportedly used and included in the analytical method were detected in at least one wristband. An additional 19 pesticide compounds were detected beyond those that were reported to be in use, highlighting the importance of measuring exposure in addition to collecting surveys and self-reported use records. The wristband method is a candidate for more widespread use in pesticide exposure and health monitoring, and in the development of evidence-based policies for human health protection in an area where food security concerns are likely to intensify agricultural production and pesticide use in the near future.

THE LIMA BEAN POD-BORER CATERPILLARS OF PUERTO RICO

Article