NPK and flavonoids affecting insect populations in Dimorphandra mollis seedlings

NPK e flavonoides afetando populações de insetos em mudas de Dimorphandra mollis

NPK and flavonoids affecting insect populations in Dimorphandra mollis seedlings

NPK e flavonoides afetando populações de insetos em mudas de Dimorphandra mollis

Germano Leão Demolin Leite^I*; Farley William Souza Silva^I; Rafael Eugênio Maia Guanabens^I; Luiz Arnaldo Fernandes^I; Lourdes Silva Figueiredo; Leonardo Ferreira Silva^I

^ILaboratório de Entomologia Universitário, Instituto de Ciências Agrárias, Universidade Federal de Minas Gerais, Av. Universitária, 1000, Cx. Postal 125, 39404-006, Montes Claros, Minas Gerais, Brazil. *Author for correspondence. E-mail: [e-mail]

ABSTRACT

The study evaluated the influence of different levels of nitrogen (N), phosphorus (P) and potassium (K), and flavonoids on the population of insects in Dimorphandra mollis Benth (Leguminosae) seedlings. The treatments associated with the highest level of attacks by Frankliniella schulzei (Trybon) (Thysanoptera: Thripidae) were 600 mg dm^-3 of P and 50 mg dm^-3 of K. The highest level of attacks by Coccidae occurred for 300 of P and 150 and 250 mg dm^-3 of K. The last two treatments also exhibited the highest level of attacks by Pseudococcidae. On the other hand, the control exhibited higher levels of flavonoids and a lower level of insect attacks. We observed a small positive effect of N levels on attack by F. schulzei. The levels of N, P and K negatively affected the levels of flavonoids in the leaves of D. mollis. We detected no significant effects of flavonoid levels on the populations of Coccidae, Pseudoccocidae and F. schulzei. Higher numbers of Coccidae and Pseudococcidae were observed in the abaxial face of apical leaves. However, higher numbers of F. schulzei were observed on the adaxial face at lower heights in the canopy. The preferred treatment for the production of D. mollis seedlings is the control (without fertilization) because it showed higher flavonoid levels than other treatments and did not result in higher insect numbers.

Keywords: “fava d’anta”, Coccidae, Pseudococcidae, Frankliniella schulzei.

RESUMO

O estudo avaliou a influência de diferentes níveis de nitrogênio (N), fósforo (P) e potássio (K) e flavonoides sobre a população de insetos em mudas de Dimorphandra mollis Benth (Leguminosae). Os tratamentos associados com maiores níveis de ataque de Frankliniella schulzei (Trybon) (Thysanoptera: Thripidae) foram 600 mg dm^-3 de P e 50 mg dm^-3 de K. Os maiores níveis de ataque de Coccidae ocorreu para 300 de P e 150 e 250 mg dm^-3 de K. Os dois últimos tratamentos também exibiram altos níveis de ataque de Pseudococcidae. Por outro lado, o controle exibiu maior nível de flavonoides e menor nível de ataque de insetos. Foi observado um pequeno efeito positivo dos níveis de N no ataque de F. schulzei. Os níveis de N, P e K afetaram negativamente os níveis de flavonoides nas folhas de D. mollis. Não foi detectado efeitos significativos dos níveis de flavonoides sobre as populações de Coccidae, Pseudoccocidae e F. schulzei. Observou-se maior número de Coccidae e Pseudococcidae na face abaxial de folhas apicais. Entretanto, maiores números de F. schulzei foram observados na face adaxial das partes mais baixas do dossel. O tratamento preferido para produção de mudas de D. mollis é o controle (sem fertilização) porque apresentou maior teor de flavonoides do que nos outros tratamentos e não apresentou maior ataque de insetos.

Palavras-chave: fava-d’anta, Coccidae, Pseudococcidae, Frankliniella schulzei.

Introduction

The use of medicinal plants to cure or to prevent disease increases each year. The cultivation of these plants and/or the extraction of substances from plants that possess therapeutic properties has become an attractive alternative for agriculture and is interesting and viable at the national level of the industry (SIMÕES et al., 2000). However, some species that show great potential for the pharmaceutical industry are not receiving sufficient attention and are little studied by the scientific community.

Among the species of the Brazilian flora that deserve more extensive study is Dimorphandra mollis Benth (Leguminosae), commonly known as “fava d’anta”, a native species of the Brazilian Savanna, found in Minas Gerais, São Paulo, Goiás, Mato Grosso and Mato Grosso do Sul (LORENZI; MATOS, 2002; PACHECO et al., 2010). The D. mollis is a deciduous pioneer tree of medium size. The bioflavonoid rutin or rutoside is extracted from its fruits in the prematuration stage (LORENZI; MATOS, 2002; LUCCI; MAZZAFERA, 2009). The proportion of rutin occurring in the dry matter can vary from 6 to 10% (HUBINGER et al., 2010; SOUZA et al., 1991). Other substances, such as rhamnose and quercetin, can also be extracted from the fruits (PETACCI et al., 2010).

Species of plants such as D. mollis that are subject to intensive extraction activities are thereby at risk for extinction. Accordingly, such species require management strategies and cultivation procedures (GONÇALVES et al., 2010; LEITE et al., 2006; VIANA E SOUZA; LOVATO, 2010). An alternative is the production of seedlings for colonization of the areas in which extractive activity occurs or for commercial plantations. This approach requires knowledge of the nutritional demands of the plants, primarily in regard to such macronutrients as nitrogen (N), potassium (K) and phosphorus (P). Consequently, the domestication of the medicinal plants is an alternative approach for the production of Phytotherapeutic substances for the industry. However, the seedlings can be attacked by insects that can affect the quantity and the quality of the product (LEITE et al., 2008).

Moreover, the fertilization of plants can influence vulnerability to insect attack (LEITE et al., 2003). Indeed, different levels of nutrients can produce physiological and morphological alterations in plants (COELHO et al., 1999; LARA, 1991). Food has very significant effects on the distribution and abundance of insects. It has direct influences on insect populations and affects biological, morphological and behavioral processes (GALLO et al., 2002). The nutrients N, P and K have important functions in plants and interfere with insect population dynamics. Previous studies of insects associated with D. mollis have investigated ants and bees in adult plants (CINTRA et al., 2002, 2005a and b; ROTHER et al., 2009).

The aim of this work is to evaluate the influence of N, P and K levels and flavonoids on the insects associated with D. mollis seedlings.

Material and methods

These studies were conducted under greenhouse conditions in the “Instituto de Ciências Agrárias da Universidade Federal de Minas Gerais (ICA-UFMG)”, Montes Claros, Minas Gerais State, from July to November 2005.

Seeds of D. mollis were subjected to scarification on the side opposite the hilum and were immersed in water for 24h. Soon thereafter, six seeds were planted in a three dm³ vase. The soil used was a dystrophic Red Latosol collected from a layer 0-20 cm deep. Soil physical and chemical properties, determined according to the methodology of Embrapa (1997), were as follows: pH in water 4.6, P = 0.6 mg dm^-3, Ca = 11.0 mmol_c dm^-3, Mg = 4.0 mmol_c dm^-3, K = 1.0 mmol_c dm^-3, Al = 37 mmol_c dm^-3, H + Al = 140 mmol_c dm^-3, S = 16.0 mmol_c dm^-3, t = 53.0, m = 70%, T = 156 mmol_c dm^-3, V = 10%, organic matter = 24 g kg^-1, sand = 500 g kg^-1, silt = 80 g kg^-1 and clay = 420 g kg^-1.

After germination, the two largest plants were chosen from each pot and the other plants eliminated. The experimental design was entirely randomized with three repetitions and 19 treatments: six levels of nitrogen (50, 100, 150, 200, 250 and 300 mg dm^-3) in the form of NH₄NO₃, six levels of phosphorus (100, 200, 300, 400, 500, 600 mg dm^-3) in the form of H₃PO₄ six levels of potassium (50, 100, 150, 200, 250 and 300 mg dm^-3) in the form of KNO₃, and the control (without fertilization).

To complement the fertilization, the nutrients Mg, S, B, Cu, Zn and Ca were used (60, 40, 0.35, 1.5, 0.5, and 200 mg dm^-3, respectively). Fertilization was performed one week before the seeds were planted. Irrigation was conducted with distilled water in order to avoid contamination and to ensure the effects of the fertilization.

The aerial part of each plant was collected after 150 days, at the beginning of December 2005. The aerial part was placed in Kraft paper bags, dried in a forced-circulation oven at 60ºC for three days until constant weight was achieved, and used for determination of dry matter. Subsequently, this material was ground in a Wiley mill (20 mesh), and the extraction of total flavonoids was performed according to Mendes et al. (2005).

The evaluations of insect occurrence (natural infestation) and of the level of damage (percent) were performed by visual inspection weekly in the morning on one leaf from the apical, medium and basal parts of the canopy of each plant, on both leaf faces. Defoliation was determined visually by estimating the percentage of leaf area lost on a scale from 0-100% by increments of 5% of the total area removed (SASTAWA et al., 2004, MIZUMACHI et al., 2006).

Regression analysis (p < 0.05) was applied to relate data on insects to N, P and K and flavonoids and to relate flavonoids to soil attributes. Data were transformed using the square root function and subjected to an analysis of variance and to the Tukey or Scott-Knott tests (p < 0.05).

Results and discussion

Scale insects of the families Coccidae and Pseudococcidae (Hemiptera) and thrips Frankliniella schulzei (Trybon) (Thysanoptera: Thripidae) were observed in D. mollis seedlings. The attack of scale insects produced honeydew on the D. mollis leaves. These families of scale insects include the pest species Coccus viridis (Green) in citrus culture and Pseudococcus adonidum (L.) in horticultural plants. Frankliniella schulzei produced scratches on the leaves of D. mollis seedlings and thereby caused leaf chlorosis. This insect is a pest species on several crops including cotton and horticultural plants (GALLO et al., 2002).

The treatments associated with the highest level of attacks by F. schulzei were 600 mg dm^-3 of P and 50 mg dm^-3 of K (Table 1). The highest level of attacks by Coccidae occurred for 300 mg dm^-3 of P and 150 and 250 mg dm^-3 of K. The last two treatments also exhibited the highest level of attacks by Pseudococcidae (Table 1). The control exhibited higher levels of flavonoids and a lower level of insect attacks (Table 1).

Excess of N or deficiency of K can cause accumulation of free amino acids and can consequently increase the populations of sucking insects on plants (JANSSON; EKBOM, 2002). Species of sucking insects such as aphids, scale, leafhoppers, whitefly and thrips and several species of phytophagous mites are not able to extract amino acids from proteins for their own use. Consequently, these insects depend on free amino acids in the plants (GALLO et al., 2002). Phosphorus can participate in cell wall synthesis. It can accordingly influence the function of the cell wall as a barrier to disease. Phosphorus can also occur in toxic compounds and can affect metabolic routes that counteract insects or diseases (MALAVOLTA, 2004). We noted a small positive effect of N levels on attack by F. schulzei (Figure 1). However, the effects of N, P and K on attacks by Coccidae and Pseudococcidae as well as the effects of P and K in relation to F. schulzei were not significant (data not shown). In other words, we did not observe a substantial effect of the levels of N, P and K on the insects. This finding perhaps results from the low population densities of insects on D. mollis seedlings (Table 1).

Dimorphandra mollis participates in a symbiosis with soil bacteria that assimilate atmospheric N (PEREIRA; OLIVEIRA, 2005). Probably for this reason, the N levels did not affect the growth of the seedlings. According to Pinto and Lameira (2001), the synthesis of compounds originating from secondary metabolism can be induced in several ways; for example, by nutritional stress. Mendes et al. (2005) also verified a reduction in the levels of total flavonoids as a function of increasing doses of P in D. mollis seedlings cultivated in nutrient-rich solution. In the present experiment, the stressed seedlings (without fertilization) produced larger quantities of secondary metabolites, including flavonoids (Figure 2). These seedlings were not preferred by the insects (Table 1). Gazzoni et al. (1997) observed higher mortality in caterpillars given a diet of mixed flavonoids (rutin and quercetin) at the highest doses.

We detected no significant effect of flavonoid levels on the scale insects (Coccidae + Pseudoccocidae) and F. schulzei populations (Figure 1). The flavonoids are probably important as an initial barrier against insects (antixenosis). Once the insects were established on the plants, they may have experienced deleterious effects on their life cycles (antibiosis). This process would explain their low density in D. mollis seedlings. In other words, the lowest level of flavonoids observed in D. mollis leaves (1.02%) could have been enough to affect these insects negatively. Macedo et al. (2002) observed a strong negative effect on Callosobruchus maculates F. (Coleoptera: Bruchidae) larvae of 1% trypsin inhibitor isolated from D. mollis seeds. According to Fernandes et al. (2004), an increase in the concentration of nitrogen in the plant reduces the concentration of substances related to defense.

These substances include carbon-rich tannins and terpenes. The quantity and quality of the soluble compounds of nitrogen produced depend on the source of nitrogen used. These compounds could induce a larger or a smaller degree of pest resistance in the plant (BORTOLI; MAIA, 1994). Therefore, the effect of NPK on the insects is both direct (nutritional value of the plant) and indirect (defense of the plant), as observed in this work.

In all the treatments, the numbers of Coccidae and Pseudococcidae observed on the abaxial face on apical leaves were higher than the numbers observed on plants in the medium and basal heights of the canopy (Table 2). However, higher numbers of F. schulzei were observed on the adaxial face of the leaves of the inferior third of the canopy (Table 2). This distribution probably resulted from competition for space and food among species. Insects, particularly sucking insects, attack the abaxial face of apical leaves because these parts of the plant are more tender (the quantities of calcium and fiber are smaller) and are of higher nutritional value (higher level of N) (SILVA et al., 1998; LEITE et al., 2002; CHAU et al., 2005; SANTOS et al., 2003).

Conclusion

Scale insects can be pests of D. mollis seedlings because they suck the sap and coat the leaf with honeydew, thereby facilitating the growth of soot mold. Thrips can also be a pest in this plant because they produce scratches on the leaves of D. mollis seedlings and therefore cause chlorosis and premature fall of leaves. The preferred treatment for the production of D. mollis seedlings is the control condition (without fertilization) because it showed higher levels of flavonoids than did other treatments and because it did not result in higher insect numbers.

References

BORTOLI, S. A.; MAIA, I. G. Influência da aplicação de fertilizantes na ocorrência de pragas. In: SÁ, M. E.; BUZZETI, S. (Ed). Importância da adubação na qualidade dos produtos agrícolas. São Paulo: Ícone, 1994. p. 53-63.

CHAU, A.; HEINZ, M.; DAVIES, F. T. Influences of fertilization on Aphis gossypii and insecticide usage. Journal of Applied Entomology, v. 129, n. 2, p. 89-97, 2005.

CINTRA, P.; MALASPINA, O.; PETACCI, F. Toxicity of Dimorphandra mollis to workers of Apis mellifera. Journal of Brazilian Chemistry Society, v. 13, n. 1, p. 115-118, 2002.

CINTRA, P.; BUENO, F. C.; BUENO, O. C.; MALASPINA, O.; PETACCI, F.; FERNANDES, J. B. Astilbin toxicity to leaf-cutting ant Atta sexdens rubropilosa (Hymenoptera: Formicidae). Sociobiology, v. 45, n. 2, p. 347-353, 2005a.

CINTRA, P.; MALASPINA, O.; BUENO, O. C.; PETACCI, F.; FERNANDES, J. B.; VIEIRA, P. C.; DA SILVA, M. F. G. F. Oral toxicity of chemical substances found in Dimorphandra mollis (Caesalpiniaceae) against honeybees (Apis mellifera) (Hymenoptera: Apidae). Sociobiology, v. 45, n. 1, p. 141-149, 2005b.

COELHO, S. A. M. P.; OLIVEIRA, D. M.; BUENO, A. F.; CALAFIORI, M. H. Efeito de potássio sobre a população de mosca-branca, Bemisia tabaci (GENN, 1889) em feijoeiro, Phaseolus vulgaris L. Ecossistema, v. 24, n. 1, p. 25-27, 1999.

EMBRAPA-Empresa Brasileira de Pesquisa Agropecuária. Centro Nacional de Pesquisa de Solos. Manual de Métodos de Análises de Solos. 2. ed. Rio de Janeiro: Embrapa, 1997.

FERNANDES, L. C.; FAGUNDES, M.; SANTOS, G. A.; SILVA, G. M. Abundance of herbivore insects associated to pequizeiro (Caryocar brasiliense). Revista Árvore, v. 28, n. 6, p. 919-924, 2004.

GALLO, D.; NAKANO, O.; SILVEIRA NETO, S.; CARVALHO, R. P. L.; BATISTA, G. C.; BERTI FILHO, E.; PARRA, J. R. P.; ZUCCHI, R. A.; ALVES, S. B.; VENDRAMIM, J. D.; MARCHINI, L. C.; LOPES, J. R. S.; OMOTO, C. Manual de Entomologia Agrícola. Piracicaba: Fealq, 2002.

GAZZONI, D. L.; HÜLSMEYER, A.; HOFFMANN-CAMPO, C. B. Efeito de diferentes doses de rutina e de quercetina na biologia de Anticarsia gemmatalis Hübner, 1818 (Lep., Noctuidae). Pesquisa Agropecuária Brasileira, v. 32, n. 7, p. 673-681, 1997.

GONÇALVES, A. C.; VIEIRA, F. A.; FIORAVANTE REIS, C. A.; CARVALHO, D. Conservation of Dimorphandra mollis Benth. (Fabaceae) based on the genetic structure of natural populations. Revista Árvore, v. 34, n. 1, p. 95-101, 2010.

HUBINGER, S. Z.; CEFALI, L. C.; VELLOSA, J. C. R.; SALGADO, H. R. N.; ISAAC, V. L. B.; MOREIRA, R. R. D. Dimorphandra mollis: an alternative as a source of flavonoids with antioxidant action. Latin American Journal of Pharmacy, v. 29, n. 2, p. 271-274, 2010.

JANSSON, J.; EKBOM, B. The effect of different plant nutrient regimes on the aphid Macrosiphum euphorbiae growing on petunia. Entomologia Experimentalis et Applicata, v. 104, n. 1, p. 109-116, 2002.

LARA, F. M. Princípios de resistência de plantas a insetos. São Paulo: Ícone, 1991.

LEITE, G. L. D.; COSTA, C. A.; ALMEIDA, C. I. M.; PICANÇO, M. Efeito da adubação sobre a incidência de traça-do-tomateiro e alternaria em plantas de tomate. Horticultura Brasileira, v. 21, n. 3, p. 448-451, 2003.

LEITE, G. L. D.; PICANÇO, M.; JHAM, G. N.; ECOLE, C. C. Effect of leaf characteristics, natural enemies and climatic conditions on the intensities of Myzus persicae and Frankliniella schulzei attacks on Lycopersicon esculentum. Arquivos do Instituto Biológico, v. 69, n. 4, p. 71-82, 2002.

LEITE, G. L. D.; PIMENTA, M.; FERNANDES, P. L.; VELOSO, R. V. S.; MARTINS, E. R. Factors affecting arthropods associated with five accessions of Brazilian ginseng (Pfaffia glomerata) in Montes Claros, Brazil. Acta Scientiarum. Agronomy, v. 30, n. 1, p. 7-11, 2008.

LEITE, G. L. D.; VELOSO, R. V. S.; ZANUNCIO, J. C.; FERNANDES, L. A.; ALMEIDA, C. I. M. Phenology of Caryocar brasiliense in the Brazilian cerrado region. Forest Ecology and Management, v. 236, n. 2-3, p. 286-294, 2006.

LORENZI, H.; MATOS, F. J. A. Plantas medicinais no Brasil: nativas e exóticas cultivadas. Nova Odessa: Instituto Plantarum, 2002.

LUCCI, N.; MAZZAFERA, P. Rutin synthase in fava d'anta: Purification and influence of stressors. Canadian Journal of Plant Science, v. 89, n. 5, p. 895-902, 2009.

MACEDO, M. L. R.; MELLO, G. C.; FREIRE, M. G. M.; NOVELLO, J. C.; MARANGONI, S.; MATOS, D. G. G. Effect of a trypsin inhibitor from Dimorphandra mollis seeds on the development ofCallosobruchus maculatus. Plant Physiology and Biochemistry, v. 40, n. 10, p. 891-898, 2002.

MALAVOLTA, E. O fósforo na planta e interação com outros elementos. São Pedro: Potafós, 2004.

MENDES, A. D. R.; MARTINS, E. R.; FERNANDES, L. A.; MARQUES, C. C. L. Produção de biomassa e flavonóides totais por fava d`anta (Dimorphandra mollis Benth) sob diferentes níveis de fósforo em solução nutritiva. Revista Brasileira de Plantas Medicinais, v. 7, n. 2, p. 7-11, 2005.

MIZUMACHI, E.; MORI, A.; OSAWA, N.; AKIYAMA, R.; TOKUCHI, N. Shoot development and extension of Quercus serrata saplings in response to insect damage and nutrient conditions. Annals of Botany, v. 98, n. 1, p. 219-226, 2006.

PACHECO, M. V.; MATTEI, V. L.; MATOS, V. P.; SENA, L. H. Moura. Germination and vigor of Dimorphandra mollis Benth. seeds under different temperatures and substrates. Revista Árvore, v. 34, n. 2, p. 205-213, 2010.

PEREIRA, J. A. A.; OLIVEIRA, C. A. Efeito do Eucalyptus camaldulensis sobre a colonização micorrítica e a nodulação em Dimorphandra mollis e Stryphnodendron adstringens, em Brasilândia, Minas Gerais. Cerne, v. 11, n. 4, p. 409-415, 2005.

PETACCI, F.; FREITAS, S. S.; BRUNETTI, I. L.; KHALIL, N. M. Inhibition of peroxidase activity and scavenging of reactive oxygen species by astilbin isolated

from Dimorphandra mollis (Fabaceae, Caesalpinioideae). Biological Research, v. 43, n. 1, p. 63-74, 2010.

PINTO, J. E. B. P.; LAMEIRA, O. A. Micropropagação e metabólicos secundários in vitro de plantas medicinais. Lavras: UFLA/FAEP, 2001.

ROTHER, D. C.; SOUZA, T. F.; MALASPINA, O.; BUENO, O. C.; SILVA, M. F. G. F.; VIEIRA, P. C.; FERNANDES, J. B. Susceptibility of workers and larvae of social bees in relation to ricinine. Iheringia Serie Zoologia, v. 99, n. 1, p. 61-65, 2009.

SANTOS, T. M.; BOIÇA JÚNIOR, A. L.; SOARES, J. J. Influência de tricomas do algodoeiro sobre os aspectos biológicos e capacidade predatória de Chrysoperla externa (Hagen) alimentada com Aphis gossypii Glover. Bragantia, v. 62, n. 2, p. 243-254, 2003.

SASTAWA, B. M.; LAWAN, M.; MAINA, Y. T. Management of insect pests of soybean: effects of sowing date and intercropping on damage and grain yield in the Nigerian Sudan savanna. Crop Protection, v. 23, n. 2, p. 155-161, 2004.

SILVA, C. C.; JHAM, G. N.; PICANÇO, M.; LEITE, G. L. D. Comparison of leaf chemical composition and attack patterns of Tuta absoluta (Meyrick) (Lepidóptera: Gelechiidae) in three tomato species. Agronomia Lusitana, v. 46, n. 2-4, p. 61-71, 1998.

SIMÕES, C. M. O.; SCHENKEL, E. P.; GOSMANN, G.; MELLO, J. C. P.; MENTZ, L. A.; PETROVICK, P. R. Farmacognosia: da planta ao medicamento. Porto Alegre: UFRGS; Florianópolis: UFSC, 2000.

SOUZA, M. P.; MATOS, M. E. O.; MATOS, F. J. A.; MACHADO, M. I. L.; CRAVEIRO, A. A. Constituintes químicos ativos de plantas medicinais brasileiras. Fortaleza: EUFC, 1991.

VIANA E SOUZA, H. A.; LOVATO, M. B.. Genetic diversity and structure of the critically endangered tree Dimorphandra wilsonii and of the widespread in the Brazilian Cerrado Dimorphandra mollis: Implications for conservation. Biochemical Systematics and Ecology, v. 38, n. 1, p. 49-56, 2010.

Received on September 22, 2010. Accepted on February 2, 2011.

License information: This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

• BORTOLI, S. A.; MAIA, I. G. Influęncia da aplicaçăo de fertilizantes na ocorręncia de pragas. In: SÁ, M. E.; BUZZETI, S. (Ed). Importância da adubaçăo na qualidade dos produtos agrícolas Săo Paulo: Ícone, 1994. p. 53-63.
• CHAU, A.; HEINZ, M.; DAVIES, F. T. Influences of fertilization on Aphis gossypii and insecticide usage. Journal of Applied Entomology, v. 129, n. 2, p. 89-97, 2005.
• CINTRA, P.; MALASPINA, O.; PETACCI, F. Toxicity of Dimorphandra mollis to workers of Apis mellifera Journal of Brazilian Chemistry Society, v. 13, n. 1, p. 115-118, 2002.
• CINTRA, P.; BUENO, F. C.; BUENO, O. C.; MALASPINA, O.; PETACCI, F.; FERNANDES, J. B. Astilbin toxicity to leaf-cutting ant Atta sexdens rubropilosa (Hymenoptera: Formicidae). Sociobiology, v. 45, n. 2,   p. 347-353, 2005a.
• CINTRA, P.; MALASPINA, O.; BUENO, O. C.; PETACCI, F.; FERNANDES, J. B.; VIEIRA, P. C.; DA SILVA, M. F. G. F. Oral toxicity of chemical substances found in Dimorphandra mollis (Caesalpiniaceae) against honeybees (Apis mellifera) (Hymenoptera: Apidae). Sociobiology, v. 45, n. 1, p. 141-149, 2005b.
• COELHO, S. A. M. P.; OLIVEIRA, D. M.; BUENO, A. F.; CALAFIORI, M. H. Efeito de potássio sobre a populaçăo de mosca-branca, Bemisia tabaci (GENN, 1889) em feijoeiro, Phaseolus vulgaris L. Ecossistema, v. 24, n. 1, p. 25-27, 1999.
• EMBRAPA-Empresa Brasileira de Pesquisa Agropecußria. Centro Nacional de Pesquisa de Solos Manual de MÚtodos de Anßlises de Solos. 2. ed. Rio de Janeiro: Embrapa, 1997.
• FERNANDES, L. C.; FAGUNDES, M.; SANTOS, G. A.; SILVA, G. M. Abundance of herbivore insects associated to pequizeiro (Caryocar brasiliense). Revista Árvore, v. 28, n. 6, p. 919-924, 2004.
• GALLO, D.; NAKANO, O.; SILVEIRA NETO, S.; CARVALHO, R. P. L.; BATISTA, G. C.; BERTI FILHO, E.; PARRA, J. R. P.; ZUCCHI, R. A.; ALVES, S. B.; VENDRAMIM, J. D.; MARCHINI, L. C.; LOPES, J. R. S.; OMOTO, C. Manual de Entomologia Agrícola Piracicaba: Fealq, 2002.
• GAZZONI, D. L.; HÜLSMEYER, A.; HOFFMANN-CAMPO, C. B. Efeito de diferentes doses de rutina e de quercetina na biologia de Anticarsia gemmatalis Hübner, 1818 (Lep., Noctuidae). Pesquisa Agropecuária Brasileira, v. 32, n. 7, p. 673-681, 1997.
• GONÇALVES, A. C.; VIEIRA, F. A.; FIORAVANTE REIS, C. A.; CARVALHO, D. Conservation of Dimorphandra mollis Benth. (Fabaceae) based on the genetic structure of natural populations. Revista Árvore, v. 34, n. 1, p. 95-101, 2010.
• HUBINGER, S. Z.; CEFALI, L. C.; VELLOSA, J. C. R.; SALGADO, H. R. N.; ISAAC, V. L. B.; MOREIRA, R. R. D. Dimorphandra mollis: an alternative as a source of flavonoids with antioxidant action. Latin American Journal of Pharmacy, v. 29, n. 2, p. 271-274, 2010.
• JANSSON, J.; EKBOM, B. The effect of different plant nutrient regimes on the aphid Macrosiphum euphorbiae growing on petunia. Entomologia Experimentalis et Applicata, v. 104, n. 1, p. 109-116, 2002.
• LARA, F. M. Princípios de resistęncia de plantas a insetos Săo Paulo: Ícone, 1991.
• LEITE, G. L. D.; COSTA, C. A.; ALMEIDA, C. I. M.; PICANÇO, M. Efeito da adubaçăo sobre a incidęncia de traça-do-tomateiro e alternaria em plantas de tomate. Horticultura Brasileira, v. 21, n. 3, p. 448-451, 2003.
• LEITE, G. L. D.; PICANÇO, M.; JHAM, G. N.; ECOLE, C. C. Effect of leaf characteristics, natural enemies and climatic conditions on the intensities of Myzus persicae and Frankliniella schulzei attacks on Lycopersicon esculentum. Arquivos do Instituto Biológico, v. 69, n. 4, p. 71-82, 2002.
• LEITE, G. L. D.; PIMENTA, M.; FERNANDES, P. L.; VELOSO, R. V. S.; MARTINS, E. R. Factors affecting arthropods associated with five accessions of Brazilian ginseng (Pfaffia glomerata) in Montes Claros, Brazil. Acta Scientiarum. Agronomy, v. 30, n. 1, p. 7-11, 2008.
• LEITE, G. L. D.; VELOSO, R. V. S.; ZANUNCIO, J. C.; FERNANDES, L. A.; ALMEIDA, C. I. M. Phenology of Caryocar brasiliense in the Brazilian cerrado region. Forest Ecology and Management, v. 236, n. 2-3, p. 286-294, 2006.
• LORENZI, H.; MATOS, F. J. A. Plantas medicinais no Brasil: nativas e exóticas cultivadas. Nova Odessa: Instituto Plantarum, 2002.
• LUCCI, N.; MAZZAFERA, P. Rutin synthase in fava d'anta: Purification and influence of stressors. Canadian Journal of Plant Science, v. 89, n. 5, p. 895-902, 2009.
• MACEDO, M. L. R.; MELLO, G. C.; FREIRE, M. G. M.; NOVELLO, J. C.; MARANGONI, S.; MATOS, D. G. G. Effect of a trypsin inhibitor from Dimorphandra mollis seeds on the development ofCallosobruchus maculatus. Plant Physiology and Biochemistry, v. 40, n. 10,         p. 891-898, 2002.
• MALAVOLTA, E. O fósforo na planta e interaçăo com outros elementos Săo Pedro: Potafós, 2004.
• MENDES, A. D. R.; MARTINS, E. R.; FERNANDES, L. A.; MARQUES, C. C. L. Produçăo de biomassa e flavonóides totais por fava d`anta (Dimorphandra mollis Benth) sob diferentes níveis de fósforo em soluçăo nutritiva. Revista Brasileira de Plantas Medicinais,    v. 7, n. 2, p. 7-11, 2005.
• MIZUMACHI, E.; MORI, A.; OSAWA, N.; AKIYAMA, R.; TOKUCHI, N. Shoot development and extension of Quercus serrata saplings in response to insect damage and nutrient conditions. Annals of Botany, v. 98, n. 1,          p. 219-226, 2006.
• PACHECO, M. V.; MATTEI, V. L.; MATOS, V. P.; SENA, L. H. Moura. Germination and vigor of Dimorphandra mollis Benth. seeds under different temperatures and substrates. Revista Árvore, v. 34, n. 2, p. 205-213, 2010.
• PEREIRA, J. A. A.; OLIVEIRA, C. A. Efeito do Eucalyptus camaldulensis sobre a colonizaçăo micorrítica e a nodulaçăo em Dimorphandra mollis e Stryphnodendron adstringens, em Brasilândia, Minas Gerais. Cerne, v. 11, n. 4, p. 409-415, 2005.
• PINTO, J. E. B. P.; LAMEIRA, O. A Micropropagaçăo e metabólicos secundários in vitro de plantas medicinais Lavras: UFLA/FAEP, 2001.
• ROTHER, D. C.; SOUZA, T. F.; MALASPINA, O.; BUENO, O. C.; SILVA, M. F. G. F.; VIEIRA, P. C.; FERNANDES, J. B. Susceptibility of workers and larvae of social bees in relation to ricinine. Iheringia Serie Zoologia, v. 99, n. 1, p. 61-65, 2009.
• SANTOS, T. M.; BOIÇA JÚNIOR, A. L.; SOARES, J. J. Influęncia de tricomas do algodoeiro sobre os aspectos biológicos e capacidade predatória de Chrysoperla externa (Hagen) alimentada com Aphis gossypii Glover. Bragantia, v. 62, n. 2, p. 243-254, 2003.
• SASTAWA, B. M.; LAWAN, M.; MAINA, Y. T. Management of insect pests of soybean: effects of sowing date and intercropping on damage and grain yield in the Nigerian Sudan savanna. Crop Protection, v. 23, n. 2,   p. 155-161, 2004.
• SILVA, C. C.; JHAM, G. N.; PICANÇO, M.; LEITE, G. L. D. Comparison of leaf chemical composition and attack patterns of Tuta absoluta (Meyrick) (Lepidóptera: Gelechiidae) in three tomato species. Agronomia Lusitana, v. 46, n. 2-4, p. 61-71, 1998.
• SIMŐES, C. M. O.; SCHENKEL, E. P.; GOSMANN, G.; MELLO, J. C. P.; MENTZ, L. A.; PETROVICK, P. R. Farmacognosia: da planta ao medicamento. Porto Alegre: UFRGS; Florianópolis: UFSC, 2000.
• SOUZA, M. P.; MATOS, M. E. O.; MATOS, F. J. A.; MACHADO, M. I. L.; CRAVEIRO, A. A. Constituintes químicos ativos de plantas medicinais brasileiras Fortaleza: EUFC, 1991.
• VIANA E SOUZA, H. A.; LOVATO, M. B.. Genetic diversity and structure of the critically endangered tree Dimorphandra wilsonii and of the widespread in the Brazilian Cerrado Dimorphandra mollis: Implications for conservation. Biochemical Systematics and Ecology, v. 38, n. 1, p. 49-56, 2010.

Publication Dates

• Publication in this collection
  10 Jan 2012
• Date of issue
  Mar 2012

History

• Received
  22 Sept 2010
• Accepted
  02 Feb 2011