Journal of Pest Science

, Volume 91, Issue 4, pp 1165–1179 | Cite as

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

  • Malick N. Ba
  • Joseph E. Huesing
  • Manuele Tamò
  • Thomas J. V. Higgins
  • Barry R. Pittendrigh
  • Larry L. Murdock


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.


Cowpea Maruca vitrata Bt-cowpea Non-target organisms West Africa Environmental risk Assessment Arthropod fauna 



This work was supported by the US Department of Agriculture Foreign Agriculture Service (USDA/FAS) Norman E. Borlaug International Agricultural Science and Technology Fellowship Program (Borlaug Fellowship Program) under Sponsor Award/Grant Number: 58-3148-2-188/106117 to Purdue University. The award was to LLM through Purdue University and administered through International Programs in Agriculture. The authors are also grateful to the African Agriculture Technology Foundation (AATF) for supporting the Bt-cowpea project, which generated the data on Cry1Ab protein expression in cowpea.


  1. Adati T, Tamò M, Yusuf SR, Downham MCA, Singh BB, Hammond W (2007) Integrated pest management for cowpea–cereal cropping systems in the West African savannah. Int J Trop Insect Sci 27:123–137Google Scholar
  2. Adati T, Tamò M, Koji S, Downham M (2012) Effect of migration and mating status of the legume pod borer, Maruca vitrata (Fabricius) (Lepidoptera: Crambidae) on the efficacy of synthetic sex pheromone traps in West Africa. In: Boukar O, Coulibaly O, Fatokun C, Lopez K, Tamò M (eds) Enhancing cowpea value chains through research advances, Proceedings of the 5th World Cowpea Research Conference. IITA, Ibadan, Nigeria, pp 260–272Google Scholar
  3. Agunbiade TA, Coates BS, Kim KS, Forgacs D, Margam VM, Murdock LL, Ba MN, Binso-Dabire CL, Baoua I, Ishiyaku MF, Tamò M, Pittendrigh BR (2012) The spatial genetic differentiation of the legume pod borer, Maruca vitrata F. (Lepidoptera: Crambidae) populations in West Africa. Bull Entomol Res 102:589–599PubMedGoogle Scholar
  4. Agyen-Sampong M (1978) Pests of cowpea and their control in Ghana. In: Singh SR, vanEmdem HF, Taylor TA (eds) Pest of Grain Legumes: ecology and control. IITA, Ibadan, pp 85–92Google Scholar
  5. Akinfenwa S (1975) Biological study of Maruca testulalis (Geyer) (Lepidoptera: Pyralidae) in the Zaria area of northern Nigeria. M.Sc. Thesis, Ahmadu Bello University, NigeriaGoogle Scholar
  6. Arodokoun DY, Tamò M, Cloutier C, Adeoti R (2003) The importance of alternative host plants for the annual cycle of the legume pod borer, Maruca vitrata Fabricius (Lepidoptera: Pyralidae). Insect Sci Appl 23:103–113Google Scholar
  7. Arodokoun DY, Tamò M, Cloutier C, Brodeur J (2006) Larval parasitoids occurring on Maruca vitrata Fabricius (Lepidoptera: Pyralidae) in Benin, West Africa. Agr Ecosyst Environ 113:320–325Google Scholar
  8. Asante SK, Jackai LEN, Tamò M (2000) Efficiency of Gryon fulviventris (Hymenoptera: Scelionidae) as an Egg Parasitoid of Clavigralla tomentosicollis (Hemiptera: Coreidae) in Northern Nigeria. Environ Entomol 29: 815–821Google Scholar
  9. Asiwe JAN (2009). Insect mediated outcrossing and geneflow in cowpea (Vigna unguiculata (L.) Walp): implication for seed production and provision of containment structures for genetically transformed cowpea. Afr J Biotechnol 8(2):226–230, ISSN 1684–5315 © 2009 Academic JournalsGoogle Scholar
  10. Asiwe JAN (2009b) Insect mediated outcrossing and geneflow in cowpea (Vigna unguiculata (L.) Walp): Implication for seed production and provision of containment structures for genetically transformed cowpea. Afr J Biotechnol 8:226–230Google Scholar
  11. Atachi P, Ahohuendo BC (1989) Comparaison de quelques paramètres caractéristiques de la dynamique des populations entre Megalurothrips sjostedti (Trybom) et Maruca testulalis (Geyer) sur une même plante hôte, le niébé. Insect Sci Appl 10:187–197Google Scholar
  12. Atachi P, Djihou ZC (1994) Record of the host plants of Maruca testulalis (Geyer) (Lepidoptera: Pyralidae) in the Republic of Benin. Ann Soc Entomol Fr 30:169–174Google Scholar
  13. Atachi P, Gnanvossou D (1989) Dynamique quantitative des populations animales: recherches préliminaires à une étude comparée des dynamiques de biomasses, d’effectifs et de production chez Maruca testulalis (Geyer) (Lep. Pyralidae) en culture de niébé dans un agrosystème du Sud Benin. Acta Oecol 10:221–239Google Scholar
  14. Addae PC, Ishyiaku M, Tignegre JB, Bationo J, Atokple IDK, Saba M, Onyekachi FN, Lawan M, Huesing J, Beach L, Higgins TJV (2017) Efficacy of cry1Ab gene to control the pod borer Maruca vitrata in cowpea. SubmittedGoogle Scholar
  15. Ba NM, Margam VM, Dabire-Binso CL, Sanon A, McNeil J, Murdock LL, Pittendrigh BR (2009) Seasonal and regional distribution of the cowpea pod borer, Maruca vitrata Fabricius (Lepidoptera: Crambidae), in Burkina Faso. Int J Trop Insect Sci 29:109–113Google Scholar
  16. Babendreier D, Reichhard B, Romeis J, Bigler F (2008) Impact of insecticidal proteins expressed in transgenic plants on bumblebee micro-colonies. Entomol Exp Appl 126:148–157Google Scholar
  17. Bal AB (1991) Action threshold for flower thrips on cowpea (Vigna unguiculata (L.) Walp.) in Senegal. Trop Pest Manage 37:363–367Google Scholar
  18. Bottenberg H, Tamò M, Arodokoun D, Jackai LEN, Singh BB, Youm O (1997) Population dynamics and migration of cowpea pests in northern Nigeria: implications for integrated pest management. In: Singh BB, Mohan-Raj DR, Dashiell KE, LE Jackai N (eds) Advances in Cowpea Research. International Institute of Tropical Agriculture and Japan International Center for Agricultural Sciences, Ibadan, pp 271–284Google Scholar
  19. Bottenberg H, Tamò M, Singh BB (1998) Occurrence of phytophagous insects on wild Vigna sp. and cultivated cowpea: comparing the relative importance of host-plant resistance and millet intercropping. Agr Ecosyst Environ 70:217–229Google Scholar
  20. Bruner SC (1930) Report of the department of entomology and phytopathology for 1929–1930. Experiment Station of Santiago de Las Vegas, Cuba, p 74Google Scholar
  21. CERA (2010) A review of the environmental safety of the Cry1Ac protein. Center for Environmental Risk Assessment. ILSI Research Foundation 1–18Google Scholar
  22. CERA (2011) A review of the environmental safety of the Cry1Ab Protein. Center for Environmental Risk Assessment. ILSI Research Foundation 1–17Google Scholar
  23. CERA (2013) A Review of the Environmental Safety of the Cry2Ab Protein. Center for Environmental Risk Assessment. ILSI Research Foundation 1–25Google Scholar
  24. Chi Y, Sakamaki Y, Tsuda K, Kusigemachi K (2003) The seasonal abundance of the Legume Pod Borer, Maruca vitrata in Kagoshima, Japan. Mem Fac Agr Kagoshima Univ 38:41–44Google Scholar
  25. Chi Y, Sakamaki Y, Tsuda K, Kusigemati K (2005) Effect of temperature on oviposition and adult longevity of the legume pod borer, Maruca vitrata (Fabricius) (Lepidoptera: Crambidae). Appl Entomol Zool 49:29–32Google Scholar
  26. Corey D, Kambhampati S, Wilde G (1998) Electrophoretic analysis of Orius insidiosus (Hemiptera: Anthocoridae) feeding habits in field corn. J Kansas Entomol Soc 71:11–17Google Scholar
  27. Coulibaly S, Pasquet RS, Papa R, Gepts P (2002) AFLP analysis of the phenetic organization and genetic diversity of Vigna unguiculata L. Walp. reveals extensive gene flow between wild and domesticated types. Theor Appl Genet 104:358–366PubMedGoogle Scholar
  28. Dabire LCB (2001) Etude de quelques parametres biologiques et ecologiques de Clavigralla tomentosicollis Stal 1855 (Hemiptera: Coreidae), punaise suceuse des gousses de niebe [Vigna unguiculata (L.) Walp.] dans une perspective de lutte durable contre l’insecte au Burkina Faso. PhD Thesis dissertation, Universite de Cocody, Abidjan, Cote d’IvoireGoogle Scholar
  29. Donald CE, Scott RP, Blaustein KL, Halbleib ML, Sarr M, Jepson PC, Anderson KA (2016) Silicone wristbands detect individuals’ pesticide exposures in West Africa. R Soc Open Sci 3:160433. PubMedPubMedCentralGoogle Scholar
  30. Dreyer H (1994) Seed damaging field pests of cowpea (Vigna unguiculata) in southern Benin, with special reference to Clavigralla tomentosicolis Stal (Het., Coreidae). PhD Thesis No. 10894, Swiss Federal Institute of Technology ZurichGoogle Scholar
  31. Duan JJ, Huesing J, Teixeira D (2007) Development of tier-I toxicity assays for Orius insidiosus (Heteroptera: Anthocoridae) for assessing the risk of plant-incorporated protectants to nontarget heteropterans. Environ Entomol 36:982–988PubMedGoogle Scholar
  32. Duan JJ, Marvier M, Huesing JE, Dively G, Huang ZY (2008) A meta-analysis of effects of Bt crops on honey bees (Hymenoptera: Apidae). PLoS ONE. Google Scholar
  33. Echendu TNC, Akingbohungbe AE (1990) Intensive free–choice and no choice cohort tests for evaluating resistance to Maruca testulalis (Lepidoptera:Pyralidae) in cowpea. Bull Entomol Res 80:289–293Google Scholar
  34. EFSA (2009) Scientific Opinion of the Panel on Genetically Modified Organisms on applications (EFSA-GMORXMON810) for the renewal of authorisation for the continued marketing of (1) existing food and food ingredients produced from genetically modified insect resistant maize MON810; (2) feed consisting of and/or containing maize MON810, including the use of seed for cultivation; and of (3) food and feed additives and feed materials produced from maize MON810, all under Regulation (EC) No 1829/2003 from Monsanto. EFSA J 1149:1–85Google Scholar
  35. Ezueh MI (1981) Nature and significance of preflowering damage by thrips to cowpea. Entomol Exp Appl 29:305–312Google Scholar
  36. FAOSTAT (2017). (retrieved on 07 September 2017)
  37. Fatokun CA (2002) Breeding cowpea for resistance to insect pests: attempted crosses between cowpea and Vigna vexillata. In: Fatokun CA, Tarawali SA, Singh BB, Kormawa PM, Tamò M (eds) Challenges and opportunities for enhancing sustainable cowpea production, Proceedings of the 3rd World Cowpea Conference. International Institute of Tropical Agriculture, Ibadan, Nigeria, pp 52–61Google Scholar
  38. Fatokun CA, Ng Q (2007) Outcrossing in cowpea. J Food Agr Environ 5:334–338Google Scholar
  39. Federici B (2007) Bacteria as biological control agents for insects: economics, engineering and environmental safety. In: Vurro M, Gressel J (eds) Novel Biotechnologies for Biocontrol agent enhancement and management. Springer, Berlin, pp 25–51Google Scholar
  40. Firempong S, Mangalit H (1990) Spatial distribution of Maruca testululis larvae on cowpea, and a sequential sampling plan for estimating larval densities. Insect Sci Appl 11:217–222Google Scholar
  41. Fohouo FNT, Ngakou A, Kengni BS (2009) Pollination and yield responses of cowpea (Vigna unguiculata L. Walp.) to the foraging activity of Apis mellifera adansonii (Hymenoptera: Apidae) at Ngaoundéré (Cameroon). Afr J Biotechnol 8:1988–1996Google Scholar
  42. Gblagada CCS (1982) Inventaire des parasites lavaires de Maruca testulalis (Geyer) sur le niebe (Vigna unguiculata (L.) Walp) et sur le pois d’angole (Cajanus cajan L. Millsp.). MS Dissertation Universite Abomey-Calavi, BeninGoogle Scholar
  43. Hill RA, Sendashonga C (2003) General principles for risk assessment of living modified organisms: lessons from chemical risk assessment. Environ Biosafety Res 2:81–88PubMedGoogle Scholar
  44. Hofmann C, Vanderbruggen H, Höfte H, Van Rie J, Jansens S, Van Mellaert H (1988) Specificity of Bacillus thuringiensis delta-endotoxins is correlated with the presence of high-affinity binding sites in the brush border membrane of target insect midguts. Proc Natl Acad Sci 85:7844–7848PubMedGoogle Scholar
  45. Huang CC, Peng WK (2001) Emergence, mating and oviposition of the bean pod borer, Maruca vitrata (F.) (Lepidoptera: Pyralidae). Formosan Entomol 21:37–45Google Scholar
  46. Huesing J, Romeis J, Ellstrand N et al (2011) Regulatory considerations surrounding the deployment of Bt-expressing cowpea in Africa: report of the deliberations of an expert panel. GM Crops 2:211–224PubMedGoogle Scholar
  47. Huignard J, Leroi B, Alzouma I, Germain JF (1985) Oviposition and development of Bruchidius atrolineatus and Callosobruchus maculatus (Coleoptera: Bruchidae) in Vigna unguiculata cultures. Insect Sci Appl 6:691–699Google Scholar
  48. Ige OE, Olotuah OF, Akerele V (2011) Floral biology and pollination ecology of cowpea (Vigna unguiculata L. Walp). Modern Appl Sci 5:74–82Google Scholar
  49. Jackai LEN, Adalla CB (1997) Pest management practices in cowpea: a review. In: Singh BB, Mohan-Raj DR, Dashiell KE, Jackai LEN (eds) Advances in cowpea research. International Institute of Tropical Agriculture and Japan International Center for Agricultural Sciences, Ibadan, pp 240–258Google Scholar
  50. Jackai LEN, Daoust RA (1986) Insect pests of cowpeas Ann Rev Entomol 31:95–119Google Scholar
  51. Jackai LEN, Ochieng RS, Raulston JR (1990) Mating and oviposition behavior of the legume pod borer, Maruca testulalis. Entomol Exp Appl 59:179–186Google Scholar
  52. Jackai LEN, Padulosi S, Ng Q (1996) Resistance to the legume pod borer, Maruca vitrata Fabricius, and the probable modalities involved in wild Vigna. Crop Prot 15:753–761Google Scholar
  53. Jepson PC, Guzy M, Blaustein K, Sow M, Sarr M, Mineau P, Kegley S (2014) Measuring pesticide ecological and health risks in West African agriculture to establish an enabling environment for sustainable intensification. Phil Trans R Soc B 369:2013049. Google Scholar
  54. Jiang XF, Zhang L, Yang H, Sappington TH, Cheng Y, Luo LZ (2016) Biocontrol of the oriental armyworm, Mythimna separata by the tachinid fly Exorista civilis is synergized by Cry1Ab protoxin. Sci Rep 6:26873. PubMedPubMedCentralGoogle Scholar
  55. Kalaitzandonakes N, Alston JM, Bradford KJ (2007) Compliance costs for regulatory approval of new biotech crops. Nat Biotechnol 25:509–511PubMedGoogle Scholar
  56. Konrad R, Ferry N, Gatehouse AMR, Babendreier D (2008) Potential effects of oilseed rape expressing Oryzacystatin-1 (OC-1) and of purified insecticidal proteins on larvae of the solitary bee Osmia bicornis. PLoS ONE. Google Scholar
  57. Kouadio D, Echikh N, Toussaint A, Pasquet RS, Baudoin JP (2007) Organisation du pool génique de Vigna unguiculata(L.) Walp.: croisements entre les formes sauvages et cultivées du niébé. Biotechnol Agron Soc Environ 11:47–57Google Scholar
  58. Krishnamurthy B (1936) The Avare pod borers, a new method of control. Mysore Agricultural Calendar and Year Book, BangaloreGoogle Scholar
  59. Kumar R, Tian JC, Naranjo SE, Shelton AM (2014) Effects of Bt cotton on Thrips tabaci (Thysanoptera: Thripidae) and its predator, Orius insidiosus (Hemiptera: Anthocoridae). J Econ Entomol 107:927–932PubMedGoogle Scholar
  60. Langyintuo A, Lowenberg-DeBoer J (2006) Potential regional trade implications of adopting Bt cowpea in West and Central Africa. Ag Bio Forum 9:111–120Google Scholar
  61. Langyintuo AS, Lowenberg-DeBoer J, Faye M, Lambert D, Ibro G, Moussa B, Kergna A, Kushwaha S, Musa S, Ntoukam G (2003) Cowpea supply and demand in West and Central Africa. Field Crop Res 82:215–231Google Scholar
  62. Lawo NC, Wäckers FL, Romeis J (2009) Indian Bt Cotton varieties do not affect the performance of cotton Aphids. PLoS One 4:e4804. PubMedPubMedCentralGoogle Scholar
  63. Li Y, Meissle M, Romeis J (2008) Consumption of Bt maize pollen expressing Cry1Ab or Cry3Bb1 does not harm adult green lacewings, Chrysoperla carnea (Neuroptera: Chrysopidae). PLoS One 3(8):e2909. PubMedPubMedCentralGoogle Scholar
  64. Li Y, Zhang Q, Liu Q, Meissle M, Yang Y, Wang Y, Hua H, Chen X, Peng Y, Romeis J (2017) Bt rice in China—focusing the nontarget risk assessment. Plant Biotechnol J 15:1340–1345PubMedPubMedCentralGoogle Scholar
  65. Liao CT, Lin CS (2000) Occurrence of the legume pod borer, Maruca testullis, Geyer (Lepidoptera: Pyralidae) on cowpea (Vigna unguiculata Walp) and its insecticidal application trial. Plant Prot Bull 42:213–222Google Scholar
  66. Lu PF, Qiao HL, Wang XP, Wang XQ, Lei CL (2007) The emergence and mating rhythms of the legume pod borer, Maruca vitrata (Fabricius, 1787) (Lepidoptera: Pyralidae). Pan-Pac Entomol 83:226–234Google Scholar
  67. Lumbierres B, Albajes R, Pons X (2012) Positive effect of Cry1Ab-expressing Bt maize on the development and reproduction of the predator Orius majusculus under laboratory conditions. Biol Control 63:150–156Google Scholar
  68. Lundgren JG, Fergen JK, Riedell WE (2008) The influence of plant anatomy on oviposition and reproductive success of the omnivorous bug Orius insidiosus. Anim Behav 75:1495–1502Google Scholar
  69. Margam VM, Coates BS, Ba MN, Sun W, Binso-Dabire CL et al (2011a) Geographic distribution of phylogenetically-distinct legume pod borer, Maruca vitrata (Lepidoptera: Pyraloidea: Crambidae). Mol Biol Rep 38:893–903PubMedGoogle Scholar
  70. Margam VM, Coates BS, Hellmich RL, Agunbiade T et al (2011b) Mitochondrial genome sequence and expression profiling for the legume pod borer Maruca vitrata (Lepidoptera: Crambidae). PLoS ONE. Google Scholar
  71. Margam VM, Coates BS, Bayles DO et al. (2011c) Transcriptome sequencing, and rapid development and application of SNP markers for the legume pod borer Maruca vitrata (Lepidoptera: Crambidae) PLoS One.
  72. Marvier M, McCreedy C, Regetz J, Kareiva P (2007) A meta-analysis of effects of Bt cotton and maize on non-target invertebrates. Science 316:1475–1477PubMedGoogle Scholar
  73. Meagher RL, Nagoshi RN, Stuhl C, Mitchell ER (2004). Larval development of Fall Armyworm (Lepidoptera: Noctuidae) on different crop plants. Florida Entomol 87(4):454–460. Doi: 10.1653/0015-4040(2004)087[0454:LDOFAL]2.0.CO;2Google Scholar
  74. Mendelsohn M, Kough J, Vaituzis Z, Matthews K (2003) Are Bt crops safe? Nat Biotechnol 21:1003–1009PubMedGoogle Scholar
  75. Murdock LL, Coulibaly O, Higgins TJV, Huesing JE, Ishiyaku MF, Sithole-Niang I (2008) Cowpea: Legume grains and forages. In: Kole C, Hall TC (eds) A compendium of transgenic crop plants. Blackwell Publishing, Oxford, pp 23–56Google Scholar
  76. Naranjo SE (2009) Impacts of Bt crops on non-target invertebrates and insecticide use patterns. CAB Rev Perspect Agric Vet Sci Nutr Nat Resour 4:23. Google Scholar
  77. Naveen V, Naik MI, Manjunatha M, Shivanna BK, Sridhar S (2009) Biology of legume pod borer, Maruca testulalis Geyer on cowpea. Karnataka J Agr Sci 22:668–669Google Scholar
  78. Ndoye M (1978) Pests of cowpea and their control in Senegal. In: Singh SR, Van Emden HF, Taylor TA (eds) Pests of grain legumes: ecology and control. International Institute of Tropical Agriculture, Ibadan, pp 113–115Google Scholar
  79. Niu L, Ma Y, Mannakkara A, Zhao Y, Ma W, Lei C, Chen L (2013) Impact of single and stacked insect-resistant bt-cotton on the honey bee and silkworm. PLoS One 8(9):e72988. PubMedPubMedCentralGoogle Scholar
  80. Ochieng RS, Okeyo-Owuor JB, Dabrowski ZT (1981) Studies on the legume pod borer, Maruca-Testulalis (Geyer): mass rearing on natural food. Insect Sci Applic 1:269–272Google Scholar
  81. OECD (2007) Consensus document on safety information on transgenic plants expressing Bacillus thuringiensis. OECD Environment, Health and Safety Publications Series on Harmonization of Regulatory Oversight in Biotechnology. ENV/JM/MONO (2007)14: OECD 2007Google Scholar
  82. Ofuya TI (1987) A population explosion of Aphis craccivora Koch (Homoptera: Aphididae) in cowpeas protected with cypermethrin. FAO Plant Prot Bull 35:75–77Google Scholar
  83. Ofuya TI (1989) The effect of pod growth stages in cowpea on aphid reproduction and damage by the cowpea aphid, Aphis craccivora (Homoptera: Aphididae). Ann Appl Biol 115:563–566Google Scholar
  84. Okeyo-Owuor JB, Ochieng R (1981) Studies on the legume pod-borer Maruca testululis (Geyer)–1: Life cycle and behavior. Insect Sci Appl 1:263–268Google Scholar
  85. Okeyo-Owuor JB, Oloo GW, Agwaro PO (1991) Natural enemies of the legume pod borer, Maruca testulalis Geyer (Lepidoptera: Pyralidae) in small scale farming systems of western Kenya. Insect Sci Appl 12:35–42Google Scholar
  86. Okwakpam BA, Youdeowei A (1980) The annotated key to four species of thrips (Thysanoptera) attacking edible legumes in Nigeria. Bull IFAN 42:157–165Google Scholar
  87. Olaifa JI, Akingbohungbe AE (1981) Aspects of the biology of the black cowpea moth, Cydia ptychora (Lepidoptera: Tortricidae) related to host plant phenology. Ann Appl Biol 97:129–134Google Scholar
  88. Onstad DW, Kang J, Ba NM, Tamò M, Jackai L, Dabire C, Pittendrigh BR (2012) Modeling evolution of resistance by Maruca vitrata (Lepidoptera: Crambidae) to transgenic insecticidal cowpea in Africa. Environ Entomol 41:1255–1267PubMedGoogle Scholar
  89. Ouedraogo AP, Sou S, Sanon A, Monge JP, Huignard J, Tran MD, Credland PF (1996) Influence of temperature and humidity on populations of Callosobruchus maculatus (Coleoptera: Bruchidae) and its parasitoid Dinarmus basalis (Pteromalidae) in two zones of Burkina Faso. Bull Entomol Res 86:695–702Google Scholar
  90. Parh IA, Taylor TA (1981) Studies on the life cycle of the cicadellid bug Empoasca dolichi Paoli, in Southern Nigeria. J Nat Hist 15:829–835Google Scholar
  91. Pasquet R, Pittendrigh B, Ishiyaku M, Baoua I, Dabire C, Ba M, Huesing J, Murdock L (2007) Addressing gene flow issues in cowpea for West Africa. North Cent Weed Sci Soc Proc 62:81Google Scholar
  92. Pasquet RS, Peltier A, Hufford MB et al (2008) Long-distance pollen flow assessment through evaluation of pollinator foraging range suggests transgene escape distances. Proc Natl Acad Sci USA 105:13456–13461PubMedGoogle Scholar
  93. Periasamy M, Schafleitner R, Muthukalingan K, Ramasamy S (2015) Phylogeographical structure in mitochondrial DNA of legume pod borer (Maruca vitrata) population in tropical Asia and sub-Saharan Africa. PLoS ONE. Google Scholar
  94. Pigott CR, Ellar DJ (2007) Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiol Mol Biol Rev 71:255–281PubMedPubMedCentralGoogle Scholar
  95. Popelka JC, Gollasch S, Moore A, Molvig L, Higgins TJV (2006) Genetic transformation of cowpea (Vigna unguiculata L.) and stable transmission to progeny. Plant Cell Rep 25:304–312PubMedGoogle Scholar
  96. Raen AZ, Dang C, Wang F, Peng YF, Ye GY (2016) Thrips-mediated impacts from transgenic rice expressing Cry1Ab on ecological fitness of non-target predator Orius tantilus (Hemiptera: Anthocoridae). J Integr Agri 15:2059–2069Google Scholar
  97. Raheja AJ (1974) Report on the insect pests of grain legumes in northern Nigeria. In: Proceedings, 1st IITA Grain Legume Improvement Workhop. International Institute of Tropical Agriculture, Ibadan, Nigeria, pp 295–299Google Scholar
  98. Raybould A (2007a) Environmental risk assessment of genetically modified crops: general principles and risks to non-target organisms. BioAssay 2:8Google Scholar
  99. Raybould A (2007b) Ecological versus ecotoxicological methods for assessing the environmental risks of transgenic crops. Plant Sci 173:589–602Google Scholar
  100. Raybould A (2010) Reducing uncertainty in regulatory decision-making for transgenic crops. More ecological research or clearer environmental risk assessment? GM Crops 1:25–31PubMedGoogle Scholar
  101. Raybould A, Quemada H (2010) Bt crops and food security in developing countries: realised benefits, sustainable use and lowering barriers to adoption. Food Secur 2:247–259Google Scholar
  102. Romeis J, Meissle M, Bigler F (2006) Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat Biotechnol 24:63–71PubMedGoogle Scholar
  103. Romeis J, Bartsch D, Bigler F et al (2008) Assessment of risk of insect-resistant transgenic crops to nontarget arthropods. Nat Biotechnol 26:203–208PubMedGoogle Scholar
  104. Romeis J, Lawo NC, Raybould A (2009) Making effective use of existing data for case-by-case risk assessments of genetically engineered crops. J Appl Entomol 133:571–583Google Scholar
  105. Romeis J, Hellmich R, Candolfi M et al (2011) Recommendations for the design of laboratory studies on non-target arthropods for risk assessment of genetically engineered plants. Transgenic Res 20:1–22PubMedGoogle Scholar
  106. Romeis J, Raybould A, Bigler F, Candolfi M, Hellmich R, Huesing J, Shelton A (2013) Deriving criteria to select arthropod species for laboratory tests to assess the ecological risks from cultivating transgenic crops. Chemosphere 90:901–909PubMedGoogle Scholar
  107. Romeis J, Meissle M, Alvarez-Alfageme F, Bigler F, Bohan DA, Devos Y, Malone LA, Pons X, Rauschen S (2014a) Potential use of an arthropod database to support the non-target risk assessment and monitoring of transgenic plants. Trangenic Res 23:995–1013Google Scholar
  108. Romeis J, Meissle M, Naranjo SE, Li Y, Bigler F (2014b) The end of a myth-Bt (Cry1Ab) maize does not harm green lacewings. Front Plant Sci 5:391. PubMedPubMedCentralGoogle Scholar
  109. Salifu AB (1992) Some aspects of the biology of the bean flower thrips Megalurothrips sjostedti (Trybom) (Thysanoptera: Thripidae) with reference to economic injury levels on cowpea (Vigna unguiculata (L.) Walp). Rev Zool Afr 106:451–459Google Scholar
  110. Sanon A, Dabiré C, Ouedraogo AP, Huignard J (2005) Field occurrence of bruchid pests of cowpea and associated parasitoids in a Sub humid zone of Burkina Faso: Importance of the infestation of two cowpea varieties at harvest. J Plant Pathol 4:14–20Google Scholar
  111. SCBD (Secretariat of the Convention on Biological Diversity) (2000) Cartagena protocol on biosafety to the convention on biological diversity: text and annexes. SCBD, MontrealGoogle Scholar
  112. Shimada N, Miyamoto K, Kanda K, Murata H (2006a) Bacillus thuringiensis insecticidal Cry1Ab toxin does not affect the membrane integrity of the mammalian intestinal epithelial cells: An in vitro study. In Vitro Cell Dev-An 42:45–49Google Scholar
  113. Shimada N, Murata H, Mikami O et al (2006b) Effects of feeding calves genetically modified corn Bt11: a clinicobiochemical study. J Vet Med Sci 68:1113–1115PubMedGoogle Scholar
  114. Singh SR, Allen DR (1980) Pests, diseases, resistance, and protection in cowpea. In: Summerfield RJ, Bunting AH (eds) Advances in Legume Science. HMSO, London, pp 419–443Google Scholar
  115. Singh SR, Jackai LEN (1985) Insect pests of cowpeas in Africa: their life cycle, economic importance and potential for control. In: Singh SR, Rachie KO (eds) Cowpea research, production and utilization. Wiley, Chichester, pp 217–231Google Scholar
  116. Singh SR, Jackai LEN (1988) Mini Review. The legume pod-borer, Maruca testulalis (Geyer): Past, present and future research. Insect Sci Appl 9:1–5Google Scholar
  117. Singh SR, Van Emden HF (1979) Insect pests of grain legumes. Annu Rev Entomol 24:255–278Google Scholar
  118. Singh SR, Jackai LEN, Dos Santos JHR, Adalla CB (1990) Insect pests of cowpea. In: Singh SR (ed) Insect pests of tropical food legumes. Wiley, Chichester, pp 43–89Google Scholar
  119. Srinivasan R (2008) Susceptibility of legume pod borer (LPB), Maruca vitrata to δ-endotoxins of Bacillus thuringiensis (Bt) in Taiwan. J Invert Path 97:79–81Google Scholar
  120. Suh JB, Jackai LEN, Hammond WNO (1986) Observations on pod sucking bug populations on cowpea at Mokwa, Nigeria. Trop Grain Legume Bull 33:17–19Google Scholar
  121. Tamò M, Baumgaertner J, Delucchi V, Herren HR (1993a) Assessment of key factors responsible for the pest status of the bean flower thrips Megalurothrips sjostedti (Thysanoptera, Thripidae) in West Africa. Bull Entomol Res 83:251–258Google Scholar
  122. Tamò M, Baumgaertner J, Arodokoun DY (1993b) The spatio temporal distribution of Megalurothrips sjostedti (Thysanoptera, Thripidae) life stages on cowpea, and development of sampling plans. Bull Soc Entomol Suisse 66:15–34Google Scholar
  123. Tamò M, Srinivasan R, Dannon E, Agboton C, Datinon B, Dabire C, Baoua I, Ba MN, Haruna B, Pittendrigh BR (2012) Biological control: a major component for the long-term cowpea pest Management strategy. In: Fatokun CA, Tarawali SA, Singh BB, Kormawa PM, Tamò M (eds) Challenges and opportunities for enhancing sustainable cowpea production, Proceedings of the 3rd World Cowpea Conference. International Institute of Tropical Agriculture, Ibadan, Nigeria, pp 249–259Google Scholar
  124. Tamò M, Pittendrigh BR, Miresmailli S, Font V, Blalock B, Dannon E, Datinon B, Agyekum M, Donovan C, Biaou E (2016) From biocontrol to precision-IPM in Africa: Challenges and opportunities. International Congress of Entomology, Orlando, Florida, 24–28 Sept, 2016. Abstract 0644:
  125. Taylor TA (1967) The bionomics of Maruca testululis Gey. (Lepidoptera: Pyralidae), a major pest of cowpeas in Nigeria. J West Africa Sci Assoc 12:111–129Google Scholar
  126. Taylor TA (1978) Maruca testulalis, an important pest of tropical grain. In: Singh SR, Van Emden HF, Taylor TA (eds) Pests of grain legumes: ecology and control. Academic Press, London, pp 193–200Google Scholar
  127. Tian J-C, Wang X-P, Long L-P, Romeis J, Naranjo SE, Hellmich RL et al (2013) Bt crops producing Cry1Ac, Cry2Ab and Cry1F do not harm the green Lacewing. Chrysoperla rufilabris. PLoSOne 8(3):e60125. Google Scholar
  128. Traore F, Ba NM, Dabire-Binso CL, Sanon A, Pittendrigh BR (2014) Annual cycle of the legume pod borer Maruca vitrata Fabricius (Lepidoptera: Crambidae) in southwestern Burkina Faso. Arthropod-Plant Inte 8:155–162Google Scholar
  129. USEPA (2007) White paper on tier-based testing for the effects of proteinaceous insecticidal plant-incorporated protectants on non-target arthropods for regulatory risk assessments. Rose R. Ed. Washington, DC: US Environmental Protection Agency Washington, DC.
  130. USEPA (2010) United States Environmental Protection Agency Biopesticide Registration Document Cry1Ab and Cry1F Bacillus thuringiensis (Bt) Corn Plant-Incorporated Protectants
  131. USEPA (2011) United States Environmental Protection Agency Biopesticide Registration Document Bacillus thuringiensis Cry1A.105 and Cry2Ab2 Insecticidal Proteins and the Genetic Material Necessary for Their Production in Corn [PC Codes 006515 (Cry2Ab2), 006514 (Cry1A.105)].
  132. Usua EJ, Singh SR (1979) Behavior of cowpea pod borer, Maruca testulalis Geyer. Nigerian J Entomol 3:231–239Google Scholar
  133. Van Rie J, Jansens S, Hofte H, Degheele D, Van Mellaert H (1989) Specificity of Bacillus thuringiensis δ-endotoxins. Eur J Biochem 186:239–247PubMedGoogle Scholar
  134. Van Rie J, Jansens S, Hofte H, Degheele D, Van Mellaert H (1990) Receptors on the brush border membrane of the insect midgut as determinants of the specificity of Bacillus thuringiensis delta-endotoxins. Appl Environ Microbiol 56:1378–1385PubMedPubMedCentralGoogle Scholar
  135. Wolcott GN (1933) The Lima bean pod borer caterpillars of Puerto Rico. J Dept Agr Puerto Rico 17:241–255Google Scholar
  136. Wolfenbarger LL, Naranjo SE, Lundgren JG, Bitzer RJ, Watrud LS (2008) Bt crop effects on functional guilds of non-target arthropods: A meta-analysis. PLoS One 3(5):e2118. PubMedPubMedCentralGoogle Scholar
  137. Wolfersberger M, Hofmann C, Luthy P (1986) Bacterial Protein Toxins. In: Falmagne P, Alouf JE, Fehrenbach FJ Jeljaszewicz J, Thelestam M (eds). Fischer, New York, 237–238Google Scholar
  138. Zhao Y, Zhan S, Luo JY, Wang CY, Lv LM, Wang XP, Cui JJ, Lei CL (2016) Bt proteins Cry1Ah and Cry2Ab do not affect cotton aphid Aphis gossypii and ladybeetle Propylea japonica. Sci Rep 6:20368. PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Malick N. Ba
    • 1
  • Joseph E. Huesing
    • 2
  • Manuele Tamò
    • 3
  • Thomas J. V. Higgins
    • 4
  • Barry R. Pittendrigh
    • 5
  • Larry L. Murdock
    • 6
  1. 1.International Crops Research Institute for the Semi-Arid TropicsNiameyNiger
  2. 2.United States Agency for International Development (USAID)WashingtonUSA
  3. 3.International Institute of Tropical AgricultureCotonouBenin
  4. 4.Commonwealth Scientific and Industrial Research Organisation (CSIRO), Agriculture and FoodCanberraAustralia
  5. 5.Department of EntomologyMichigan State UniversityEast LansingUSA
  6. 6.Department of EntomologyPurdue UniversityWest LafayetteUSA

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