c resistance The identification of C. maculatus 15 Inoculation of BRS Acauã For BRS Tapaihum cultivar, Rita de Cassia Nunes a C. maculatus. C. maculatus. -amylase inhibitors. 𝛽 These studies have mostly focused on the identi- 14 7 – 12 , 8 reared on beans from four cowpea cultivars fertilized Paulo Ivan Fernandes-Júnior, b Correspondence to: Luciana Barboza Silva, Crop Sciences Department,University Federal of Piauí,64900-000, Campus Brazil. E-mail: Professora [email protected] Cinobelina Elvas, Bom Jesus,Crop Piauí Sciences Department,Cinobelina Federal Elvas, Bom University Jesus, Piauí, of Brazil Piauí, Campus Professora Agricultural, Environmental and Biological Sciences Center,of Federal Recôncavo University da Bahia, Cruz das Almas, Bahia, Brazil Embrapa Semiárido, Petrolina, Pernambuco, Brazil Agronomy Department, UNESP, Campus de Ilha Solteira, Sao Paulo, Brazil Weevil resistance has been studied in several cowpea c a ∗ d b these methods may present risks for humanof health and re-infestation carry by a the risk pestpopulations. due to the development of resistant cultivars. fication of cultivars thatdue have developed to trypsin and cowpea resistance sources and their specificis defense important compounds in the determination of which genetic improvements Callosobruchus 6 – 3 Cal- 2 , 1 d Callosobruchus maculatus control; however, 10 – Gabriel dos Santos Carvalho, 7 a* Rafaela S A Nóbrega, C. maculatus a on cowpea grains is dependent is considered the main pest of stored cow- : 4276–4280 www.soci.org © 2016 Society of Chemical Industry 96 C. maculatus. and Bruno E Pavan a 2016; inoculation; nitrogen fertilization; stored grain Farmers use chemicals for

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A portion of the grains and seeds produced in each harvest Inoculation of cowpea seeds with commercial inoculants helps peas because it causesthe quantitative insect and larvae enter qualitative the losses beanseggs. and when leave behind droppings and losobruchus maculatus cannot be used, mainly due to pest attacks during storage. to establish plants in the field and can increase grain yield. J Sci Food Agric Keywords: Recent studies performed in theulation north-east of region of cowpeas Brazil, with inoc- resulted efficient in nitrogen-fixing yields similar rhizobia to strains thosetion, observed indicating with that nitrogen the use fertiliza- of inoculants issource an for alternative cowpea nitrogen producers of this region. inoculation with diazotrophic bacteriamortality among strains BR3267, BR 3262 andCONCLUSION: BR BRS Tapaihum 3299, and BRS and Acauã cultivars nitrogenof showed the population fertilization lowest cumulative growth, resulted insect and emergence inrhizobial and the strains. instantaneous higher rates highest insect mortality,© 2016 mainly Society when of Chemical the Industry grains were obtained from plants inoculated with INTRODUCTION Cowpea [Vigna unguiculatatant (L.) low-cost Walp] and high-quality (Fabaceae) proteinical is source, regions especially an such in as impor- trop- In Africa, Brazil, South this America andtems, legume mainly Central those is small America. farmers very with family-basednorth-east important systems in and to the north the regions.ond For production Piauí most sys- State, economically cowpea important is legume,232 000 occupying the ha an sec- with area 44 000 of tons produced in the year 2012. BACKGROUND: Beans from cowpea cultivars fertilizeddifferent with nitrogen mineral N concentrations and or nitrogen inoculated with metabolitepests. various composition, In rhizobium which strains this affects may study, the contain the beans’with defense population different mechanisms growth against nitrogen of sources wasnitrogen evaluated. sources: The mineral factors tested N(absolute were control). fertilization, beans inoculation from four with cowpea five cultivars strains and of sevenRESULTS: BRS different symbiotic Tapaihum and BRS diazotrophic Acauã cultivars bacteria, had lowerof and cumulative the emergence soil and insects instantaneous rate nitrogen compared of with populationcultivar growth other with cultivars, the indicating diazotrophic antixenosis bacteria resistance strain against BR 3299 resulted in higher mortality of Abstract on the plant genotype Elida Barros Torres, Luciana Barboza Silva, The damage caused by maculatus (wileyonlinelibrary.com) DOI 10.1002/jsfa.7639 Research Article Received: 6 May 2015 Revised: 13 November 2015 Accepted article published: 21 January 2016 Published online in Wiley Online Library: 5 April 2016 Marinho

4276 4277 Zabrotes The differences were 18 However, for this variable, wileyonlinelibrary.com/jsfa As reported in the literature, 17 . 21 infestation then the other two . 0.05. This measure was positively corre- 0.05) between cultivars and inocu- < 20 < P P C. maculatus C. maculates test, and averages were compared using the C. maculatus F . 19 . Higher emergence of adult insects results in higher 19 14 C. maculatus 0.05) (Table 2). The instantaneous rate of population growth 7 factorial scheme, with four replicates per treatment. The fac- < The experimental design was completely randomized with a A significant interaction ( A loss of mass in stored beans is an important parameter to mea- Regarding the cowpea genotype, BRS Acauã and BRS Tapaihum The lowest instantaneous rates of population growth were × P 4 SNK test with using the SAS 8.02 software. tors tested were beans from four cowpea cultivarsTapaihum, (BRS BRS Acauã, Carijó BRS and BRS Pujante),gen and sources: mineral seven N different fertilisation, inoculation nitro- with symbioticzotrophic dia- bacteria (strains BR 3267, BR 3262,and BR UFLA 3299, 03–84), INPA 03-11B and soil nitrogentilization (absolute or control, inoculation without with fer- rhizobial strains).jected The to data an were analysis sub- of variance.were Interactions tested between using an treatments was positive for all tested cultivars,ceptible indicating to that they attack were by sus- lation was observed for the cumulative insectity survival (Table and 1). mortal- The lowest values of cumulative insect survival after sure both from an economicalof cultivar point resistance of to pests. view and as an indicator the cultivars BRS Acauãthan and for BRS the other Tapaihum plant showed genotypes,as pointing lower less out levels these susceptible genotypes to RESULTS AND DISCUSSION A significant effect was observedgence, on absolute the cumulative dry insect biomass emer- of consumed population and growth instantaneousconditions. rate between A different significant interaction cowpea betweengen cultivars cultivars sources was and and observed nitro- formortality the (Table cumulative 1). insect survival and cultivars had a negative effect on insectdecreased development, cumulative resulting emergence in (Table 2). Thecultivars remaining supported tested insect emergence andconditions may provide for favorable insect development.gence The may decreased result from insectwith high emer- insecticidal larvae potential, such mortality as vicilin, caused whichlegumes. is by present proteins in some the high levels of trypsinagainst inhibitors are responsible for resistance observed for BRS Acauãrates and were BRS significantly Tapaihum different( cultivars from and the these other cultivars tested subfascuatus quantitative damage, loss oftive bean effects nutritional on quality, and beanfor nega- appearance, commercialization which and consumption. makes The themindicate results of unsuitable that this study BRSantixenosis Acauã resistance, and or BRS non-preference, towhat Tapaihum the was cultivars pests, observed similar exhibited to for the BRS Nova Era cultivar with lated with the number ofresulted emerged insects, from i.e. higher higher consumption, emergence orthe presence negatively of correlated substances capable with of inhibitingof the consumption the seed interior by considered significant when cultivars evaluated in this study.population This growth, lower observed instantaneous rate with of theprobably data due from to this the study,inhibit insect was presence feeding, such of as arcelin substances orliterature. vicilin, in as expressed the in the grains that ) 0 = i 20 r . Grains 16 resistance split into two 1 − is the time inter- t C. maculatus Vigna unguiculata Δ indicates population C. maculatus. i is the final number of r f C. maculatus N -resistant plants. ,where 5% relative humidity with a 12-h t indicates population growth, ± Δ i in grains of four different cowpea r )]/ o C. maculatus N C, 60 / f ∘ N 2 : 4276–4280 © 2016 Society of Chemical Industry ± [ln( 96 ), which was calculated according to the follow- = i i r r C. maculatus 2016; 17 C for 15 days to eliminate infestations arising from the is the initial number of insects, and ∘ o 20 N − After 60 days, the jars were opened, and the following variables The beans were exposed to the 28 treatments (four cultivars and The goal of the present study was to evaluate the population Following harvest, beans were placed in plastic bags and were Insects were obtained from a breeding stock and kept in closed by performing a no-choicegrowth. The assay bioassay was performed and in plastic analyzing jarsin that the diameter were 10 and population cm 6 cm in height.and The lids wrapped of the in jars were voile perforated grams fabric to of enable cowpea ventilation.non-sexed beans One adult from hundred insects with the agesplaced different ranging in from each treatments 1 jar. to and 5 20 days were were quantified: number of emerged insects (alivegrain and dead), mass, final consumed bean mass andulationgrowth( instantaneous rate of pop- photoperiod. Insects were fed cowpeathat grains originated ( from producers fromPiauí. the Bom Jesus municipality, seven nitrogen sources) were tested for indicates stable population, and a negative parameters of cultivars that were inoculatedfertilized with with mineral nitrogen different for testing rhizobial thebeans hypothesis: strains cowpea from or plants fertilized with differentmore sources resistant of to nitrogen attack are or are susceptible to decline heading towards extinction. J Sci Food Agric MATERIAL AND METHODS For this experiment weBRS used Tapaihum, BRS four Pujante cowpea andsown cultivars: BRS in BRS Carijó. the When field, Acauã, the theystrains were seed inoculated of were with diazotrophic one bacteria: of(SEMIA the BR 6464), following BR 3267 3299, (SEMIA INPA 03-11B 6463),(SEMIA (SEMIA 6462), BR 6461). or 3262 Two UFLA 03–84 non-inoculatedperformed: control one treatments with were urea fertilization also (80 kg N ha The damage caused by C. maculates on cowpeacouldbemadetoobtain www.soci.org applications, one at planting andemergence) one and 30 an days absolute following control seedling withoutulation fertilization with or rhizobia. inoc- The fieldMandacaru experiment Experiment was Station, Juazeiro, conducted Bahia at state (BA), the Brazil,the at Embrapa Semiárido premises. left at field. Prior to conducting the experiment, the beansfrom were removed the freezer, placed infabric plastic and containers, kept in covered the withreach laboratory voile the hygroscopic for balance 6 for days each cultivar. to allow the seeds to 3 L plastic containerswrapped with with perforated voile lids. fabricescape The to of containers allow gas were insects exchangeand or and were entrance kept avoid at the of 27 undesirable biological agents val in days. A positive value of ing equation: from cowpea cultivars fertilized with mineralrhizobial N strains or inoculated may with have differenttrations nitrogen and metabolite compositions. concen- Increasing thelegumes nitrogen may availability result in insuch higher as flavonoids, production alkaloids, of terpenes and defense sterols,turn which molecules, bolster would in the defense mechanismsbeans with against different pests levels of and resistance result against in insects, i r The et al. ,Vari- 27 , NS NS 26 et al. : 4276–4280 96 0.000069 0.000063 0.01 *significant < 14 . lineage (IT81D-1053) P 2016; Instantaneous rate of population growth, was dependent on the NS C. maculatus NS (Boh.), and vicilin was observed J Sci Food Agric Vigna unguiculata It should be highlighted that the . C. maculatus biomass (g) 25 Consumed dry larvae Thus, applying bacterial inoculation as a nitrogen 9 Zabrotes subfasciatus Furthermore, arcelin was observed to inhibit the devel- 0.05). 24 C. maculatus 23 < ant vicilins from a resistant P (absolute number) Plant nutrition may also result in bean tegmental resistance. The Insects completely depend on resources acquired dur- It should be noted that there were significant differences in Cumulative mortality 1 Oliveira GB, Kunz D, Peres TV, Leal RB, Uchôa AF, Samuel R, effects. cowpea cultivars and nitrogenAcauã cultivars sources. showed BRS the Tapaihum lowestand and cumulative instantaneous insect BRS emergence rates ofinsect population mortality, growth, and mainlyplants the inoculated when highest with rhizobial the strains. grains were obtained from to interfere in the development of opment of higher insect mortalityBRS observed Tapaihum for whenshould cultivars provided BRS be with Acauãzotrophic further certain and bacteria, studied nitrogen inand addition given sources to the that decreasing environmentalalso inoculation production impacts be costs with used ofpesticides. dia- for nitrogen pest fertilization, control, can thereby decreasing the use of source may be associated withmay changes stimulate the in production cowpea of defense nutrition substancesIt and in may the be grains. stated that thegen quantity and compounds quality produced of the depend solublethat nitro- on different sources the will induce nitrogen variable levelsto source of pests. plant and resistance tegument is where the attackline by of bruchids defense starts against and infestation. isdifferences Research a results in physical reported plant that tegumentseclosion resulted and in adult emergence varied and rates theto time of perforate needed the for larvae tegument. the larvae ing the larval stages for survival and reproduction. the grain Ngen concentration ( between different sources of nitro- REFERENCES CONCLUSIONS The infestation caused by decreased survival ofstudy therefore adult indicates insectsvars possible to observed resistance in of the cowpea culti- present Nitrogen sources: diazotrophic bacteria strains (BR 3262, BR 3267, UFLA b reared for 60 days on beans from different cowpea cultivars that were either www.soci.org EB Torres C. mac- i reared r a a b ab 758 085.6** 712 044.0* 76.76 0.077 0.076 0.071 476 629.26* 1 482 800.7** 5.95 © 2016 Society of Chemical Industry 0.073 growth, population (absolute number) Cumulative survival test. Instantaneous rate of F Callosobruchus maculatus a a a b 53.0 56.7 56.4 41.3 allosobruchus maculatus NS NS Consumed biomass (g) number) a a Cumulative b ab . emergence (absolute , as indicated by the cumulative insect emer- emergence Cumulative (absolute number) df Biological parameters of C ANOVA of biological parameters of C. maculatus 22 C. maculatus 0.05; NS, not significant, according to the when cowpea beans from BRS Acauã cultivar were inocu- < 0.05. P Averages followed by the same letter within the same column were Cowpea cultivars: BRS Acauã, BRS Carijó, BRS Pujante, BRS Tapaihum. < Cul(C)N(T) 3 6 1 723 014* 938 580 10 093 474** 10 049 471** 1 462.43** 0.000206* a The quantity, quality and proportion of nutrients present in BRS Acauã and BRS Tapaihum cultivars were the most resistant not significantly different according toP the SNK test, with a cut-off of 03–84, INPA 0311B and BR 3299), mineral nitrogen (C/N), and soil nitrogen (control). Cultivar for 60 days onassay: beans Bom from Jesus, PI different 2013 cowpea cultivars in a no-choice a,b BRS AcauãBRS TapaihumBRS CarijóBRS 1620.7 1698.9 Pujante 2027.1 2131.7 Table 2. Two types of control were used: with or without mineral nitrogen. Bom Jesus, PI, 2013. CV, coefficient of variation **significant at C*TErrorCV%Average 18 111 – – 597 433 511 646 1 869.6 38.3 195 628.3 969.4 45.6 366 106.3 889.1 59.81193 68.1 0.0000539 51.8 14.9 0.0741 9.9 FV a b inoculated with different strains of nitrogen fixing bacteria or were not inoculated (controls) at Table 1. the food (includingor nitrogen) anti-nutritional and compounds theous (allelochemicals) impacts presence can on of the haveto secondary biology vari- contribute of insects, to which the affect next their generation ability and may have sublethal wileyonlinelibrary.com/jsfa lated with the diazotrophicBRS bacteria Tapaihum strain cultivar BR inoculated 3299.and with Beans BR strains 3299 from and BR3267, fertilizedinsect BR with mortality. 3262 urea Non-protein also factors, had suchacids, higher as may cumulative tannins interfere and with phytic theand nervous metabolism system, of hormonal balance theliterature. plant’s natural enemies, as reported in ulatus 60 days of storagetilization were and observed the for non-fertilized and BRSBRS Tapahium, non-inoculated the Acauã lowest controls. cumulative with insect For survival urea wasfor observed fer- grains from plants inoculated with3267 the (Table strains 3). BR The 3262 results andthe BR obtained sources of with nitrogen this supply work usedbia indicate strains here or (inoculation that nitrogen with fertilization) rhizo- hadsurvival an of hormoligosis effect on against gence and instantaneous rateis of worth population noting growth that (Table there 2). was It an increased mortality of

4278 4279 Bb Cal- Aa Aa Ba Aa Bc Ab Bbc Revista Calloso- Calloso- Neotrop J Sci Food 63.8 1469 1903 581 1166 515.8 218 1383 :779–785 J Sci Food . 35 ssp. [Associ- Callosobruchus Zabrotes subfas- :315–320 (1997). Aa Bab (Boh.) (Coleoptera: 26 Bc ABb Ac Ab Aab Aa Zabrotes subfasciatus Feijão-caupi: Avanços SAS Institute, Cary, NC Sitophilus 184.8 887.0 123.8 1187.0 1177 412.0 2063 (cowpea) seeds to Vigna unguiculata wileyonlinelibrary.com/jsfa :1068–1073 (1997). 16 (L.) Walp., on the development of a 1570.3 Aa A Aa Aba Ab Bb Cb :729–745 (2003). ssp.]. MSc thesis. Universidade Estadual Db Zabrotes subfasciatus , Composição bioquímica da semente 30 (Fabricius) (Coleoptera: Bruchidae)]. 1545.5 908.0 1518.0 104.3 32.0 515.8 144.5 2151.5 Pesquisa Agropecuária Brasileira et al. Vigna unguiculata is restricted to cotyledonary tissues. L., to ]. Sitophilus ed. by Freire-Filho FR, Lima JAA and Ribeiro VQ. da Sociedade Entomológica do Brasil SAS User’s Guide: Statistics v. 8.2. Vigna unguiculata (Fabricius) (Coleopetar: Bruchidae) [Effect of cowpea :77–83 (2004). Environ Toxicol Chem Funct Plant Biol Aa Aa 33 :1977–1985 (2006). :948–958 (1989). Aba Aa Bab Aab Aa :70–77 (2011). (Boheman, 1833) (Coleoptera: Chrysomelidae: Bruchinae) Db 6 86 30 , Resistance of Nitrogen source 1550.5 883.3 1857.0 614.0 48.3 411.8 310.5 855.3 b [Biochemical compositionTecnológicos of seeds],Embrapa in Informação(2005). Tecnológica, Brasília, DF, pp. 338–365 losobruchus maculatus Entomol EA, Cajazeiras JB, bruchus maculatus Agric Biochemical basis of insect resistance in icological endpoints: the intrinsic (rm) and instantaneousincrease. (ri) rates of (2001). cia de genótiposciatus de feijão-caupi[Resistance ao of cowpea ataque genotypes to de attack(Boheman, by 1833) (Coleoptera: Chrysomelidae:Verde Bruchinae)]. gos Entomopatogenicos para controle de ation of resistant cornthe varieties control and of entomopathogenicdo fungi Oeste for do(2006). Paraná, Marechal Cândido Rodon Campus,unguiculata Paraná (L.) Walp., sobre omaculatus desenvolvimento de genotypes, bruchus maculatus (2000). et al. Agric nous metabolites as signals and protectantsopment. in early seedling devel- Bruchidae)]. ao caruncho [Resistance of cowpea genotypes to (Coleoptera: Bruchidae) [Resistance ofPhaseolus cultivars vulgaris and lines of bean, adults reared for 60 days on beans from different cowpea cultivars that 22 Grangeiro TB, Castellón RER, Araújo FMMC, Silva SMS, Freire 15 Gatehouse AMR, Gatehouse JA, Dobie P, Kilminster AM and Boutlier D, 17 Walthall WK and Stark JD, Comparison of two population-level ecotox- 18 SAS Institute, 19 Barbosa DRS, Fontes LS, Melo RS, Rocha LÍR and Lima MS, Resistên- 20 Potrich M, Associação de variedades resistentes de milho e fun- 21 Costa NP and Boiça JRAL, Efeito de genótipos de caupi, Vigna 14 Domingues SJS, Melo FR, Aguiar JM, Affonso AG, Giuli JSA, Rose JL, 16 Ndakidemi PA and Dakora FD, Legume seed flavonoids and nitroge- 13 Barreto PD and Quinderé AW, Resistência de genótipos de caupi Aa Aa Aa Aa ABa Aa BCb Aab 904.0 928.3 1768.8 759.0 2092.3 1164 235.2 1743.8 Vigna Vigna (Boh.) C. maculatus :364–369 J Agric Sci 5 Ab Aa Aa Levantamento Bc Ac Cb Aab Cb (L.) Walp. por 1303.3 248.3 1867.0 148.5 361.8 914.3 138.0 1872.3 larval midgut epithe- :1519–5228 (2005). 5 http://www.ibge.gov.br/ :1–19 (2014). Afr J Biotechnol (Nairobi) 0.05. Callosobruchus maculatus < 45 < Zabrotes subfasciatus P Bc Ac Cb Ab Aa Aa Aab ABb [Systematic Survey of Agricul- L. a Pesquisa Agropecuárea Brasileira :395–402 (2014). :45–52 (2014). :1–7 (2011). Vigna unguiculata 49 42 168 Callosobruchus maculatus , Performance of polymer compositions as carrier Revista Brasileira de Ciências Agrárias : 4276–4280 © 2016 Society of Chemical Industry :333–339 (2003). Phaseolus vulgaris 96 et al. 38 (L.) Walp, family farming in Piauí, Brazil. Revista Ciência Agronômica (L.) Walp. inoculated with rhizobia strains in Bom Jesus, , Contribution of biological nitrogen fixation to cowpea: a 2016; , Field perfomace of new cowpea cultivars inoculated with Cumulative insect survival and mortality (average) of et al. Comp Biochem Physiol B Revista Ciência Agronômica et al. Revista de Biologia and Ciências da Terra :2945–2951 (2012). :178–184 (2015). :153–160 (2013). unguiculata 11 and Pacheco LP, Biological nitrogen fixation in production of to cowpea rhizobial inoculantpre-inoculated formulations: seeds survival and of field rhizobia efficiency. in 5 Sistemático de Produçãotural Agrícola Production] Piauí (2013). Available: home/estatistica/indicadores/agropecuaria/lspa. [July 2013]. MCP, strategy for improving grain yieldBiol Fertil in Soil the semi-arid region of Brazil. Rumjanek NG, symbiotically fixed by glicidiatem and in cowpea semiarid in Northeast50 an Brazil. agroforestry sys- and Silva JAL,inoculado com Produtividade bactérias diazotróficas do simbióticas no feijão-caupicv Piauí [Cowpea cv BR17 BR Gurguéiabacteria 17 yield in Gurguéia Piauí]. inoculated(2010). with symbiotic diazotrophic Nodulação e produtividade de accumulate inside lium. cepas de rizóbio em Bom Jesus, PI [Yield and nodulation of unguiculata PI]. ST, JS, Eficiência simbiótica de progenitoresfeijão-caupi. de cultivares brasileiras de Bioactivity of vegetal(Coleoptera: Bruchidae) powders in caupi against bean andsis. seed physiological analy- e linhagens de efficient nitogen-fixing rhizobialPesquisa strains Agropecuária Brasileira in the Brazilian Semiarid. Nitrogen source: diazotrophic bacteria strains (BR 3262, BR 3267, UFLA 03–84, INPA 0311B and BR 3299), mineral nitrogen (C/N) and soil nitrogen Cowpea cultivars: BRS Acauã, BRS Carijó, BRS Pujante and BRS Tapaihum. Cutivar BR 3267 BR 3262 BR 3299 UFLA 03-84 INPA 03-11B C/N N soil were either inoculated with different strains of nitrogen fixing bacteria or non-inoculated (controls) a b BRS PujanteTwo types of controls were utilised:Averages with followed or by without the the same addition upper-caseaccording of letter to mineral within the nitrogen. the SNK Bom test, same Jesus, with PI row a 2013. and cut-off lower-case of letter within the same column were not significantly different 1803 BRSTapaihmBRS Carijó 122 294 BRTapaihumBRS CarijóBRS PujanteCumulative insect mortality BRS Acauã 141.0 2068 218.5 453.8 Cumulative insect survival BRS Acauã 1024 a Table 3. (control). 5 Ferreira LVM, Nóbrega RSA, Nóbrega JCA, Aguiar FL, Moreira FMS 3 Martins LMV, Rangel FW, Xavier GR, Ribeiro JRA, Morgado LB, Neves 4 Fernandes JPI, Silva Júnior EB, Silva Júnior S, Santos CERS, Oliveira PJ, 8 Costa EM, Nóbrega RSA, Martins LV, Amaral FHC and Moreira FMS, 6 Martins JCR, Freitas ADS, Menezes RSC and Sampaio EVSB, Nitrogen 7 Almeida ALG, Alcântara RMCM, Nóbrega RSA, Nóbrega JCA, Leite lFC 2 Instituto Brasileiro de Geografia e Estatística (IBGE), 9 Marinho RCC, Nobrega RSA, Zilli JE, Xavier GR, Santos CAF, Aidair J Sci Food Agric The damage caused by C. maculates on cowpea www.soci.org 10 Alcantrara RMCM, Xavier GR, Rumjanek NG, Rocha MM and Carvalho 11 Sousa AH, Maracajá PB, Silva RMA, Moura AMN and Andrade12 WG, Wanderley VS, Oliveira JV and Andrade Jr ML, Resistência de cultivares Crop et al. : 4276–4280 96 Songklanakarin J Sci 2016; . Oxford University Press, New (Coleoptera: Bruchidae) larvae. J Sci Food Agric (Fabricius) in chickpea genotypes on the :287–291 (2012). :651–657 (2011). The Evolution of Life Histories , Natural seed coats provide protection against penetration 34 30 et al. Callosobruchus maculatus York, p. 264 (1992). Callosobruchus maculatus basis of various parameters during storage. SC, by Protect Technol 27 Sarwar M, Assessment of resistance to the attack of bean beetle 25 Souza AJ, Santos PO, Pinto MST, Wermelinger TT, Ribeiro ES, Souza 26 Stearns SC, www.soci.org EB Torres ,ed.by Biotecnologia © 2016 Society of Chemical Industry Importância Da Adubação Na Qualidade Dos Produtos , ed. by Sá ME and Buzzeti S. São Paulo, Brazil, pp. 53–63 Panizzi AR and Parra JRP. EmbrapaDF, pp. informação 1107–1139 tecnológica, Brasília, (2009). ocorrência de pragasoccurrence], in [Influence ofAgrícolas fertiliser application on(1994). pest base para onutrition manejo as basis integrado for integrated de pest management], pragas in [Bioecology and insect e nutrição de insetos. Base para manejo integrado de pragas wileyonlinelibrary.com/jsfa 24 Bortoli AS and Maia IG, Influência da aplicação de fertilizantes na 23 Parra JRP and Panizzi ARA, Bioecologia e a nutrição de insetos como

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