Services on Demand
Print version ISSN 0301-8059
An. Soc. Entomol. Bras. vol.29 no.3 Londrina Sept. 2000
Oviposition preference of Bemisia tabaci (Genn.) biotype B (Homoptera: Aleyrodidae) for bean genotypes containing arcelin in the seeds
Preferência para oviposição de Bemisia tabaci (Genn.) biótipo B (Homoptera: Aleyrodidae) por genótipos de feijoeiros portadores de arcelina nas sementes
Maria A. de G. OrianiI; Fernando M. LaraII
IDept° de Entomol., Fitopatol. e Zoologia Aplicada, ESALQ/USP, Caixa postal 9, 13418-900, Piracicaba, SP, Brasil
IIDept° de Fitossanidade, FCAV/UNESP, Rod. Carlos Tonanni, km 5, 14870-000, Jaboticabal, SP, Brasil
The oviposition preference of Bemisia tabaci biotype B (Homoptera: Aleyrodidae) for bean (Phaseolus vulgaris L.) genotypes containing arcelin in the seeds was evaluated. The tests were carried out under greenhouse conditions, in the dry and wet seasons, with the following genotypes: ARC 3s, ARC 5s (wild genotypes containing arcelin in the seeds); ARC 1, ARC 2, ARC 3, ARC 4 (near isogenic lines containing arcelin in the seeds - EMBRAPA) and Porrillo 70, Bolinha, IAPAR MD 808 (commercial genotypes without arcelin). In the free choice and no-choice oviposition tests, Bolinha and Porrillo 70 genotypes were preferred for oviposition by that insect. The Bolinha susceptibility could be related to the great number of acicular trichomes presents on its leaves surface. The wild genotypes, ARC 5s and ARC 3s, showed oviposition nonpreference resistance type. This resistance is not related to the arcelin variants, since the bred genotypes also contain arcelin in its seeds and did not show resistance to B. tabaci, biotype B.
Key words: Insecta, Phaseolus vulgaris, whitefly, antixenosis, trichomes.
Genótipos de feijoeiro (P. vulgaris) que contêm arcelina em suas sementes foram avaliados quanto à preferência para oviposição de Bemisia tabaci biótipo B (Homoptera: Aleyrodidae). Os testes foram conduzidos em condições de estufa, nas épocas "das águas" e "da seca", em dois anos consecutivos, com os seguintes genótipos: ARC 3s, ARC 5s (genótipos selvagens portadores de arcelina); ARC 1, ARC 2, ARC 3, ARC 4 (linhagens quase-isogênicas portadoras de arcelina - EMBRAPA), Porrillo 70, Bolinha e IAPAR MD 808 (cultivares sem arcelina). Nos ensaios de preferência para oviposição, em teste com e sem chance de escolha, observou-se que os genótipos Bolinha e Porrillo 70 foram os mais preferidos para oviposição pelo inseto. A suscetibilidade do genótipo Bolinha pode estar relacionada com o grande número de tricomas aciculares presentes em suas folhas. Os genótipos selvagens, ARC 5s e ARC 3s, apresentaram resistência do tipo não-preferência para oviposição. Esta resistência não está relacionada com a arcelina, uma vez que os genótipos melhorados também contêm arcelina em suas sementes e não mostraram-se resistentes a esse biótipo de B. tabaci.
Palavras-chave: Insecta, Phaseolus vulgaris, mosca branca, antixenose, tricomas.
Beans (Phaseolus vulgaris L.) are the primary sources of protein for the diet of many people in the Tropics. Bemisia tabaci (Genn.) is supposed to be one of the most harmful pests that attacks bean crops. These insects damage the plants by extracting large quantities of phloem sap and transmitting the bean golden mosaic virus (Costa et al. 1973). This disease can induce bean yield losses ranging from 40 to 100% (Faria & Zimmermann 1987, Faria et al. 1994). Recently, a new biotype of B. tabaci, biotype B, also referred to as B. argentifolli (Bellows & Perring) has been associated with high yield losses in several crops. Distinct biological differences have been documented for the two biotypes: biotype B lays significantly more eggs (Bethke et al. 1991, Costa & Brown 1991), ingests greater quantities of plant sap during feeding and consequently excretes greater volumes of honeydew (Byrne & Miller 1990) and has greater host range than the biotype A (Bedford et al. 1994). Furthermore, biotype B induces phytotoxic disorders, such as: squash silverleaf in cultivars of Cucurbitaceae (Costa & Brown 1991, Costa et al. 1993, Jiménez et al. 1995), uneven ripening in tomato (Schuster et al. 1990) and white stem streaking in cole crops (Brown et al. 1991). In 1991, the biotype B of B. tabaci was first reported in Brazil infesting tomato, broccoli, eggplant and pumpkin crops (Lourenção & Nagai 1994). The aim of this study was to determine the oviposition preference of B. tabaci for bean genotypes containing arcelin in the seeds.
Material and Methods
All trials were carried out in Host Plant Resistance to Insects Laboratories, Department of Entomology, and in an area of the Teaching and Research Farm of Faculdade de Ciências Agrárias e Veterinárias/Universidade Estadual Paulista. The genotypes containing arcelin were obtained from the Centro Nacional de Pesquisa do Arroz e do Feijão/EMBRAPA. The following genotypes of P. vulgaris were used: ARC 3s and ARC 5s (wild genotype containing arcelin 3 and 5, respectively); ARC 1, ARC 2, ARC 3 and ARC 4 (genotypes bred by EMBRAPA containing arcelin 1, 2, 3 and 4, respectively); Porrillo 70, IAPAR MD 808 and Bolinha. The seeds were planted in plastic pots containing three parts of soil, one part of sand and one part of organic compound. The plants were watered daily and fertilized as recommended for the crop. When tests were set up, adults of B. tabaci biotype B reared on tomato, broccoli and Brassica oleracea L. were collected by mouth vacuum apparatus. The infestation took place when bean plants were 21 day-old, characterized by Azael (1976) as stages IV-2 and/or IV-3. After infestation, four leaves were collected of each repetition and the number of eggs laid on the abaxial surface of leaves was counted.
All experiments were carried out under greenhouse conditions and repeated two times with 10 replications, in the wet and dry seasons. Data were submitted to ANOVA test and the means were compared by Tukey test (P < 0,05). When necessary, the original data were transformed to x1/2 or (x + 0.5)1/2.
Free-Choice Test. Each replication consisted of a pot with two bean plants. In the 1995 dry season trial, a free-choice trial in a randomized block design was set up using cages (2x2x2 m) covered by nylon netting into which approximately 6.000 adults were released having the choice among all nine bean genotypes during four days. For the other trials, the pots with bean plants were transferred to a greenhouse containing broccoli infested by B. tabaci, in a completely randomized design and remained there during 24 hours.
No-Choice Test. After sowing, each pot was placed in individual cage (60 cm high and 40 cm diameter) covered by fine mesh nylon clothes. In the 1995 trials, a pot with two bean plants was infested by 200 insects during four days, while in the 1996/97 trials, each pot contained just one bean plant was infested by 200 insects during five days.
Taking into account the previous free and no-choice tests, another no-choice trial was also carried out with the following genotypes: ARC 3s and ARC 5s (resistant genotypes) and Porrillo 70 and Bolinha (susceptible ones). All trials were set up in a completely randomized design.
Trichomes Density. The number of hooked and acicular trichome (assessed by counting the number of hairs in an area of 9.6 mm2, using a stereomicroscope with clear chamber) was determined at two locations (close to the petiole and at the tip of the leaflet) on the fully expanded central leaflet of the second trifoliolate. Trichome density was calculated as the average densities at those two locations. The methodology was adapted of McAuslane (1996). Ten replicates were performed for each genotype.
Results and Discussion
Free-Choice Tests. The mean density of eggs was significantly lower on ARC 5s genotype followed by ARC 3s, in all free-choice tests (Table 1). In the wet season, the Bolinha genotype showed the highest number of eggs laid on its leaves, in both years tested. In the dry season, Bolinha (1995 trials), and ARC 4, Bolinha, ARC 2 and Porrillo 70 (1996 trials) were the most preferred genotypes. The ovipositional preference results indicate the ARC 5s genotype was the least preferred by B. tabaci and Bolinha was the most preferred one in most trials.
The trichome density on bean leaves was measured since Peña et. al. 1992, Peña et. al. 1993a, Heinz & Zalom 1995, McAuslane et al. 1995, McAuslane et al. 1996 and others authors detected the influence of trichomes on ovipositional preference of B. tabaci.
All three types of trichomes were present on the surface of each cultivar (Fig. 1). According to Dahlin et al. (1992), the morphological characteristics of common bean trichomes were described as follow: the acicular type is long (400 mm) and straight (Fig. 1B); the hooked type is smaller (200 mm) (Fig. 1B) and the glandular is short (60 mm) (Fig. 1A). The density of the latter one was not measured since no influence has been detected on B. tabaci oviposition preference.
As shown in Table 2, the number of total trichomes/cm2 was lower on ARC 3, Porrillo 70, ARC 4, ARC 1 and IAPAR MD 808 genotypes (from 116.2 to 167.2 trichomes/cm2) and significantly greater on ARC 5s (791.2 trichomes/cm2), Bolinha (643.2 trichomes/cm2) and ARC 3s (552.6 trichomes/cm2) genotypes.
The hooked trichomes were the most common on bean leaves, with values varying from 114.6 to 790.1 trichomes/cm2, representing 95.8% to 100% of total trichomes. On Bolinha genotype, the hooked trichome represented 70% of total pubescence density. The number of acicular trichome was significantly higher on Bolinha genotype (157.8 trichomes/cm2), while all others genotypes had only a range of 0 to 5.7 trichomes/cm2 (Table 2). The acicular trichome is found mainly on the central vein and on the primary and secondary veins of the leaves. Since such areas were avoided during evaluation, all genotypes had small number of acicular trichome, except for Bolinha genotype, which possesses acicular trichome in other areas besides the veins.
The large number of eggs laid by B. tabaci on Bolinha genotype in the free-choice tests (Table 1) could be related to the great number of acicular trichomes present on its leaves surface (Table 2). Peña et al. (1993b) verified that B. tabaci showed oviposition preference for 27-R and PC-50 genotypes, which had longer acicular trichomes, while A-429 and DOR-303 genotypes (shorter acicular trichomes) had the smallest oviposition. Although several researchers had reported that hooked trichomes can confer resistance in bean genotypes by preventing the attack of Empoasca fabae (Pillemer & Tingey 1976, 1978) and Liriomyza trifolii (Fagoonee & Toory 1983, Quiring et al. 1992), it was not possible to find any relation between these trichomes and oviposition preference by B. tabaci. Peña et al. (1993b) reported that such mechanism seems not to constitute an effective defense towards B. tabaci oviposition.
No-Choice Tests. In the wet season, the wild genotypes ARC 3s and ARC 5s showed significantly less eggs on leaves surface than Porrillo 70 (1995 trial) and ARC 2, ARC 4, ARC 1 and ARC 3 (1996 trial) (Table 3). In the dry season, considering both years, the wild genotypes showed smaller number of eggs laid on its leaves and Porrillo 70 was the most preferred one.
To confirm the resistance index showed by bean genotypes studied in previous free and no-choice tests, two resistant (ARC 3s and ARC 5s) and two susceptible genotypes (Bolinha and Porrillo 70) were selected. The wild genotypes ARC 5s and ARC 3s were the least preferred for oviposition by B. tabaci and Bolinha and Porrillo 70 were the most oviposited ones (Table 4).
The ARC 5s and ARC 3s genotypes showed oviposition nonpreference resistance type, with emphasis on ARC 5s. Lara (1997) reported that Mexican bean weevil Zabrotes subfasciatus also had oviposition nonpre- ference for those genotypes. Thus, it suggests that the wild genotypes express multiple resistance, that is, they show resistance to two or more insects species (Lara 1991).
It is important to mention that this resistance is not related to the presence of arcelin, since the bred genotypes (ARC 1, ARC 2, ARC 3 and ARC 4) also possess arcelin in their seeds and did not show resistance to B. tabaci. In addiction, if the resistance was linked to the arcelin, the ARC 3 and ARC 3s genotypes, which present the same arcelin variant (arcelin 3), should show such resistance. Another factor must be related with the wild genotype resistance, which was not transferred to the bred genotypes. This way, the ARC 5s and ARC 3s genotypes should be used for breeding program towards B. tabaci biotype B.
The authors are grateful to Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) and to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for a research fellowship, to EMBRAPA, which provided the bean seeds and to Dra. Maria Regina V. de Oliveira, who identified the insect species.
Azael, A. 1976. Numerical characterization of the development of the bean plant (Phaseolus vulgaris L.). Turrialba 26: 209-210. [ Links ]
Bedford, I.D., R.W. Briddon, J.K. Brown, R.C. Rosell & P.G. Markham. 1994. Geminivirus transmission and biological characterization of Bemisia tabaci (Gennadius) biotypes from different geographic regions. Ann. Appl. Biol. 125: 311-325. [ Links ]
Bethke, J.A., T.D. Paine & G.S. Nuessly. 1991. Comparative biology, morpho- metrics, and development of two population of Bemisia tabaci (Homoptera, Aleyrodidae) on cotton and poisettia. Ann. Entomol. Soc. Amer. 84: 407-411. [ Links ]
Brown, J.K., H.S. Costa & F. Laemmlen. 1991. First incidence of whitefly-associated aquash silverleaf (SSL) of Cucurbita and of white streaking (WSt) disorder of cole crops in Arizona and California. Plant Dis. 76: 426. [ Links ]
Byrne, D.N. & W.B. Miller. 1990. Carbohydrate and amino acid composition of phloem sap and honeydew produced by Bemisia tabaci. J. Insect Physiol. 36: 433-439. [ Links ]
Costa, A.S., C.L. Costa & H.F.G. Sauer. 1973. Surto de mosca-branca em culturas do Paraná e São Paulo. An. Soc. Entomol. Brasil 2: 20-30. [ Links ]
Costa, H.S. & J. K. Brown. 1991. Variation in biological characteristics and esterase patterns among populations of Bemisia tabaci, and the association of one population with silverleaf symptom induction. Entomol. Exp. Appl. 61: 211-219. [ Links ]
Costa, H.S., J.K. Brown, S. Sivasupra- maniam & J. Bird. 1993. Regional distribution, insecticide resistance, and reciprocal crosses between the A and B biotypes of Bemisia tabaci. Insect Sci. Appl. 14: 255-266. [ Links ]
Dahlin, R.M., M.A. Brick & J.B. Ogg. 1992. Characterization and density of trichomes on three common bean cultivars. Econ. Bot. 46: 299-304. [ Links ]
Fagoonee, I. & V.Toory. 1983. Preliminary investigations of host selection mechanisms by the leafminer Liriomyza trifolii. Insect Sci. Appl. 4: 337-341. [ Links ]
Faria, J.C. & M.J.O. Zimmermann. 1987. Controle do mosaico dourado do feijoeiro (Phaseolus vulgaris) pela resistência varietal e inseticidas. Fitopatol. Bras. 13: 32-35. [ Links ]
Faria, J.C., M.N. Oliveira & M. Yokoyama. 1994. Resposta comparativa de genótipos de feijoeiro (Phaseolus vulgaris) a inoculação com o vírus do mosaico dourado no estágio de plântulas. Fitopatol. Bras. 19: 566-572. [ Links ]
Heinz, K.M. & F.G. Zalom. 1995. Variation in trichome-based resistance to Bemisia argentifolii (Homoptera, Aleyrodidae) oviposition on tomato. J. Econ. Entomol. 88: 1494-1502. [ Links ]
Jiménez, D.R., R.K. Yokomi, R.T. Mayer & J.P. Shapiro. 1995. Cytology and physiology of silverleaf whitefly-induced squash silverleaf. Physiol. Mol. Plant Pathol. 46: 227-242. [ Links ]
Lara, F.M. 1991. Princípios de resistência de plantas a insetos. 2.ed. São Paulo, Ícone. 336p. [ Links ]
Lara, F.M. 1997. Resistance of wild and near isogenic bean lines with arcelin variants to Zabrotes subfasciatus (Boheman). I. Winter crop. An. Soc. Entomol. Brasil 26: 551-560. [ Links ]
Lourenção, A.L. & H. Nagai. 1994. Surtos populacionais de Bemisia tabaci no Estado de São Paulo. Bragantia 53: 53-59. [ Links ]
McAuslane, H.J. 1996. Influence of leaf pubescence on ovipositional preference of Bemisia argentifolii (Homoptera, Aleyrodidae) on soybean. Environ. Entomol. 25: 834-841. [ Links ]
McAuslane, H.J., F.A. Johnson, D.L. Colvin & B. Sojack. 1995. Influence of foliar pubescence on abundance and parasitism of Bemisia argentifolii (Homoptera, Aleyrodidae) on soybean and peanut. Environ. Entomol. 24: 1135-1143. [ Links ]
McAuslane, H.J., S.E. Webb & G.W. Elmstrom. 1996. Resistance in germplasm of Cucurbita pepo to silverleaf, a disorder associated with Bemisia argentifolii (Homoptera, Aleyrodidae). Fla. Entomol. 79: 206-221. [ Links ]
Peña, E.A., A. Pantoja & J. Beaver. 1992. Determinación de la pubescencia de cuatro genotipos de habichuela, Phaseolus vulgaris L. J. Agric. Univ. P. R. 76: 71-82. [ Links ]
Peña, E.A., A. Pantoja & J. Beaver. 1993a. Desarrollo de Bemisia tabaci Gennadius en cuatro genotipos de Phaseolus vulgaris L. con diferentes grados de pubescencia. J. Agric. Univ. P. R. 77: 61-67. [ Links ]
Peña, E.A., A. Pantoja, J. Beaver & Armstrong, A. 1993b. Oviposicion de Bemisia tabaci Genn. (Homoptera, Aleyrodidae) en cuatro genotipos de Phaseolus vulgaris L. (Leguminosae) con diferentes grados de pubescencia. Folia Entomol. Mex. 87: 1-12. [ Links ]
Pillemer, E.A. & W.M. Tingey. 1976. Hooked trichomes: a physical barrier to a major agricultural pest. Science 193: 482-484. [ Links ]
Pillemer, E.A. & W.M. Tingey. 1978. Hooked trichomes and resistance of Phaseolus vulgaris to Empoasca fabae (Harris). Entomol. Exp. Appl. 24: 83-94 [ Links ]
Quiring, D.T., P.R. Timmins & S.J. Park. 1992. Effect of variations in hooked trichome densities of Phaseolus vulgaris on longevity of Liriomyza trifolii (Diptera: Agromyzidae) adults. Environ. Entomol. 21: 1357-1361. [ Links ]
Schuster, D.J., T.F. Mueller, J.B. Kring & J.F. Price. 1990. Relationship of the sweetpotato whitefly to a new tomato fruit disorder in Florida. Hortscience 25: 1618-1620. [ Links ]