SCIENTIA AGRICOLA

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CONTENTS

AGRICULTURAL ENGINEERING ECOLOGY

713-720 Broiler and swine production: welfare 764-771 Agriculture, habitat loss and spatial patterns of legislation scenario human occupation in a biodiversty hotspot Produção de frangos de corte e suínos: cenário Agricultura, perda de hábitat e padrões espa- da legislação sobre bem-estar animal ciais de ocupação humana em um “hotspot” de Raquel Baracat Tosi Rodrigues da Silva; Irenilza de Alencar biodiversidade Nääs; Daniella Jorge de Moura José Alexandre Felizola Diniz-Filho; Guilherme de Oliveira; Fábio Lobo; Laerte Guimarães Ferreira; Luis Mauricio ANIMAL SCIENCE AND PASTURE Bini; Thiago Fernando Lopes Valle Brito Rangel

721-732 772-779 Potential of the seedling community of a forest Components of the leaf area index of marandu fragment for tropical forest restoration palisadegrass swards subjected to strategies of Potencial da comunidade de plântulas de um intermittent stocking fragmento florestal para a restauração de flo- Componentes do índice de área foliar de pastos restas tropicais de capim-marandu submetidos a estratégias de Ricardo Augusto Gorne Viani; Ricardo Ribeiro Rodrigues lotação intermitente Alessandra Aparecida Giacomini; Sila Carneiro da Silva; Daniel Oliveira de Lucena Sarmento; Cauê Varesqui ENTOMOLOGY Zeferino; Júlio Kuhn da Trindade; Salim Jacaúna Souza Júnior; Vítor del’Alamo Guarda; André Fischer 780-787 Marigold (Tagetes erecta L.) as an attractive crop Sbrissia to natural enemies in onion fields Cravo-de-defunto (Tagetes erecta L.) como cultura 733-741 Growth of marandu palisadegrass subjected to atrativa para inimigos naturais em cultivo de cebola strategies of intermittent stocking Luís Cláudio Paterno Silveira; Evoneo Berti Filho; Leonardo Crescimento do capim-marandu submetido à Santa Rosa Pierre; Fernanda Salles Cunha Peres; Julio estratégias de lotação intermitente Neil Cassa Louzada Alessandra Aparecida Giacomini; Sila Carneiro da Silva; Daniel Oliveira de Lucena Sarmento; Cauê Varesqui GENETICS AND PLANT BREEDING Zeferino; Salim Jacaúna Souza Júnior; Júlio Kuhn da Trindade; Vítor del’Alamo Guarda; Domício do Nascimento 788-792 Inheritance of resistance to Fusarium oxysporum Júnior f. sp. phaseoli Brazilian race 2 in common bean Controle genético da resistência à raça brasi- 742-750 Ruminal methane emission by dairy cattle in leira 2 de Fusarium oxysporum f. sp. phaseoli no Southeast Brazil feijoeiro Emissão de metano ruminal por bovinos leitei- Mônica Juliani Zavaglia Pereira; Magno Antonio ros no sudeste do Brasil Patto Ramalho; Ângela de Fátima Barbosa Abreu Márcio dos Santos Pedreira; Odo Primavesi; Magda Aparecida Lima; Rosa Frighetto; Simone Gisele de Oliveira; PLANT PATHOLOGY Telma Teresinha Berchielli 793-799 Tomato yellow vein streak virus: relationship with 751-756 Vitamin A in diets for Nile Tilapia Bemisia tabaci biotype B and host range Vitamina A em dietas para Tilápia do Nilo Tomato yellow vein streak virus: interação com a Daniela Ferraz Bacconi Campeche; Rodrigo Ramos Bemisia tabaci biótipo B e gama de hospedeiros Catharino; Helena Teixeira Godoy; José Eurico Possebon Ana Carolina Firmino; Valdir Atsushi Yuki; Adriana Cyrino Gonçalves Moreira; Jorge Alberto Marques Rezende

CROP SCIENCE SOILS AND PLANT NUTRITION

757-763 Phenology and reproductive traits of peaches and 800-805 Chemical and physical fertility indicators of a nectarines in Central-East Argentina weakly-structured Ultisol after liming and mulching Fenologia e comportamento reprodutivo de pês- Indicadores de fertilidade de um Argissolo es sego no centro-leste da Argentina truturalmente frágil sob efeito da calagem e da Norberto Francisco Gariglio; Marisa Mendow; Marcela cobertura morta Emilce Weber; María Alejandra Favaro; Diego Esteban Emanoel Gomes de Moura; Kátia Pereira Coelho; Idelfonso González-Rossia; Rubén Andrés Pilatti Colares de Freitas; Alana das Chagas Ferreira Aguiar 806-811 Cattle manure fertilization increases fig yield NOTE Adubação com esterco de curral na produção da figueira 827-830 Cultivation of Agaricus blazei ss. Heinemann using Sarita Leonel; Marco Antonio Tecchio different soils as source of casing materials Cultivo de Agaricus blazei ss. Heinemann usan- 812-818 Nitrogen availability, leaf life span and nitrogen do diferentes solos como fonte de material para conservation mechanisms in leaves of tropical a camada de cobertura trees Félix Gonçalves de Siqueira; Eustáquio Souza Dias; Romildo Disponibilidade de nitrogênio, longevidade da Silva; Emerson Tokuda Martos; Danny Lee Rinker foliar e mecanismos de conservação de nitrogênio em folhas de espécies arbóreas REVIEW tropicais 831-843 Brazilian greenhouse gas emissions: the importance Guilherme Nascimento Corte; Patrícia Macchiaverni; Inácio of agriculture and livestock Maria Dal Fabbro; Claudia Regina Baptista Haddad Emissões de gases do efeito estufa do Brasil: importância da agricultura e pastagem 819-826 Hillslope curvature, clay mineralogy, and Carlos Clemente Cerri; Stoecio Malta Ferreira Maia; phosphorus adsorption in an Alfisol cultivated with Marcelo Valadares Galdos; Carlos Eduardo Pellegrino sugarcane Cerri; Brigitte Josefine Feigl; Martial Bernoux Curvaturas de relevo, mineralogia da argila e adsorção de fósforo em Argissolo cultivado com 845 Author Index cana-de-açúcar Diogo Mazza Barbieri; José Marques Júnior; Luis Reynaldo 847 Reviewers Ferracciú Alleoni; Fernando José Garbuio; Livia Arantes Camargo Instructions to Authors 845

SCIENTIA AGRICOLA

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INDEX OF AUTHORS

Abreu, A.F.B., 788 Macchiaverni, P., 812 Aguiar, A.C.F., 800 Maia, S.M.F., 831 Alleoni, L.R.F., 819 Marques Júnior, J., 819 Barbieri, D.M., 819 Martos, E.T., 827 Berchielli, T.T., 742 Mendow, M., 757 Bernoux, M., 831 Moreira, A.G., 793 Berti Filho, E., 780 Moura, D.J., 713 Bini, L.M., 764 Moura, E.G., 800 Camargo, L.A., 819 Nääs, I.A., 713 Campeche, D.F.B., 751 Nascimento Júnior, D., 733 Catharino, R.R., 751 Oliveira, G., 764 Cerri, C.C., 831 Oliveira, S.G., 742 Cerri, C.E.P., 831 Pedreira, M.S., 742 Coelho, K.P., 800 Pereira, M.J.Z., 788 Corte, G.N., 812 Peres, F.S.C., 780 Cyrino, J.E.P. 751 Pierre, L.S.R., 780 Dias, E.S., 827 Pilatti, R.A., 757 Diniz-Filho, J.A.F., 764 Primavesi, O., 742 Fabbro, I.M.D., 812 Ramalho, M.A.P., 788 Favaro, MA., 757 Rangel, T.F.L.VB., 764 Feig, B.J., 831 Rezende, J.A.M., 793 Ferreira, L.G., 764 Rinker, D.L., 827 Firmino, A.C., 793 Rodrigues, R.R., 772 Freitas, I.C., 800 Sarmento, D.O.L., 721, 733 Frighetto, R., 742 Sbrissia, A.F., 721 Galdos, M.V., 831 Silva, R., 827 Garbuio, F.J., 819 Silva, R.B.T.R., 713 Gariglio, N.F., 757 Silva, S.C., 721, 733 Giacomini, A.A., 721, 733 Silveira, L.C.P., 780 Godoy, H.T., 751 Siqueira, F.G., 827 González-Rossia, D.E., 757 Souza Júnior, S.J., 721, 733 Guarda, V.D.A., 721, 733 Tecchio, M.A., 806 Haddad, C.R.B., 812 Trindade, J.K., 721, 733 Leonel, S., 806 Viani, R.A.G., 772 Lima, M.A., 742 Weber, M.E, 757 Lobo, F., 764 Yuki, V.A., 793 Louzada, J.N.C., 780 Zeferino, C.V., 721, 733 780 Silveira et al.

MARIGOLD (Tagetes erecta L.) AS AN ATTRACTIVE CROP TO NATURAL ENEMIES IN ONION FIELDS

Luís Cláudio Paterno Silveira1; Evoneo Berti Filho2*; Leonardo Santa Rosa Pierre2; Fernanda Salles Cunha Peres3; Julio Neil Cassa Louzada4

1 UFLA - Depto. de Entomologia, C.P. 37 - 37200-000 - Lavras, MG - Brasil. 2 USP/ESALQ - Depto. de Entomologia e Acarologia, C.P. 09 - 13418-900 - Piracicaba, SP - Brasil. 3 UNESP/FCAV - Depto. de Fitossanidade - 14884-900 - Jaboticabal, SP - Brasil. 4 UFLA - Depto. de Biologia. *Corresponding author

ABSTRACT: Onion is the third most grown vegetable crop in São Paulo state, Brazil. Organic onion farming is expected to increase in the state due to the increasing demand. Pest management in organic onion farming is based on plant extracts with insecticide effects. However, the efficacy of such plant extracts has not been proved yet, and it was observed that they do negatively affect natural enemies. Plants surrounding onion fields, and that are attractive to natural enemies, may be a good option to farmers, since they may lead to increased diversity of species and, consequently, the natural control of pest populations. This study deals with the effect of marigold plants as a resource plant to natural enemies in onion fields. The experiment was set in a certified organic farm using marigold rows at a center of an onion field. Samples were taken from marigold and the onion plants 5 m (near) and 30 m (far) from the flowering strips. Higher numbers of arthropod pests were observed in onion plants 30 m from the marigold strip, while higher numbers of predators and parasitoids were found at 5 m distance. Species richness and Shannon’s diversity index were higher at 5 m from marigold. Therefore, marigold rows next to onion fields resulted in higher number of entomophagous species, potentially enhancing the natural control of onion pests. In the study field, marigold strips may be an alternative to crop sprays for organic control of onion pests. Key words: natural control, conservation, predator, parasitoid

CRAVO-DE-DEFUNTO (Tagetes erecta L.) COMO CULTURA ATRATIVA PARA INIMIGOS NATURAIS EM CULTIVO DE CEBOLA

RESUMO: A cebola é a terceira hortaliça mais cultivada em São Paulo, cujo cultivo orgânico tende a crescer devido ao grande mercado consumidor existente. O manejo das pragas na cebolicultura orgânica baseia-se nos extratos de plantas inseticidas que, além de terem eficiência não comprovada, podem afetar negativamente os inimigos naturais. A utilização de plantas atrativas a inimigos naturais no entorno dos cultivos de cebola pode ser uma boa opção para os produtores, pois potencialmente aumentam a diversidade da artropodofauna e podem regular naturalmente as populações de espécies pragas. Verificou-se o efeito de linhas de cravo-de-defunto (Tagetes erecta L.) como cultura atrativa a inimigos naturais em campos de cebola. O experimento foi realizado em propriedade orgânica certificada, instalando-se linhas de cravo-de-defunto nas bordaduras de dois campos de cebola. Os tratamentos foram definidos coletando-se amostras nas plantas de cebola próximas às linhas da atrativa (5m) e distante das linhas (30 m). De maneira geral, observou-se maior quantidade de artrópodes fitófagos nas plantas de cebola longe da faixa atrativa e, inversamente, maior quantidade de inimigos naturais próximos à faixa. A riqueza de espécies também foi maior nas coletas próximas, o mesmo valendo para o índice de diversidade de Shannon. Portanto, a manutenção de linhas de cravo-de-defunto próximas ao cultivo de cebola promoveu maior riqueza e diversidade de artrópodes, bem como maior número de entomófagos, resultando em menor presença de fitófagos nas plantas, auxiliando na regulação natural das pragas da cultura. Palavras-chave: controle natural, conservação, predador, parasitóide

INTRODUCTION ganic vegetable crop in São Paulo state, occupying an area of 10,000 hectares (Camargo et al., 2006). It is Onion (Allium cepa L.) is the third most grown largely used for food and medicinal purposes and vegetable crop and the sixteenth most important or- chemical free bulbs therefore have greater value

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(Alonso, 1998). Because of the high market value of MATERIAL AND METHODS these products, the Brazilian growers are increasing the area of onion crops (Martins et al., 2006). The experiment was set in an organic onion field Among the pests causing yield losses in on- of 5,000 square meters, in a certified organic farm (cer- ion production in Brazil, the onion , Thrips tified by ‘Mokiti Okada Foundation’, FMO), in tabaci Lind. (Thysanoptera: Thripidae) is responsible Fernando Prestes, state of São Paulo, Brazil for 45% of onion yield losses in the country (Boiça (21°14’0.29"S; 48°40’15.61"W), from August to Oc- Júnior & Domingues, 1987; Sato, 1989; Gonçalves, tober 2004. Seedlings, compost and biofertilizer were 1996). One of the main recommendations for organic produced at the farm, and an irrigation system was farming is the recovery of functional biodiversity, used. Marigold seed was obtained directly from field which is lost or very reduced in conventionally grown collection on the organic farm selected and because monocultures. Through polycultivation, maintenance the grower has cultivated it for years, there is no way of volunteer plant species and use of attractive plants to determine the cultivar. the diversity of beneficial can be recovered The onion field has 50 × 100 m and was divided in agroecosystems (Gliessman, 2001; Altieri et al., in two similar areas by a 4 m wide path. Along the 2003). This diversity may lead to increased pest con- borders of this path, on both sides, there was a 50 m trol in onion, reducing the use of plant extracts that long and 0.5 m wide row of marigold plants. Such ar- have been shown to be detrimental to natural enemy rangement allowed the collection of onion samples at populations. varying distances from marigold plants. We sampled A plant that is potentially useful to maintain arthro- onion plants at 5 m (near) 30 m (far) and in the mari- pod biodiversity, including certain species of predator gold plant strip. Sampling began two weeks after thrips, is the marigold (Tagetes erecta L.). According transplanting when seedlings were 30 day-old, and con- to Sampaio et al. (2008) this plant hostages species tinued for the following seven weeks. Ten random of Orius (Hemiptera: Anthocoridae), which is the main samples on onion according to each distance were thrips predator around the world, including Brazil taken weekly for seven weeks (n = 140), each sample (Silveira et al., 2003a,b, 2004). Additionally, marigold corresponding to 1 m2 of the onion field. plants in-between rows of onion crop have been Onion plants were shaken against a white plastic shown to promote the reduction of aphid, nematode tray to dislodge , which were immediately and populations and virus diseased plants transferred to plastic containers and kept in 60% etha- (Martowo & Rohama, 1987; Abid & Magbool, 1990; nol for later identification. Arthropods were identified Zavaleta-Mejia & Gomes, 1995). Moreover marigold to the lowest possible level and grouped as phytopha- plants host other phytophagous species that are alter- gous or entomophagous. We performed an ANOVA native prey for entomophagous species. Some organic with the average calculated over seven weeks of sam- growers seed marigold for its pollen and nectar, which pling, showing patterns of weekly abundance but per- increase natural enemy fecundity and survival (Baggen, formed statistical analysis for the whole period of the 1999). Therefore it is important to know the richness, experiment. We used the software Statistica® for the abundance and diversity of arthropod species found analysis and SigmaPlot® for graphics. in this plant, and on the surroundings of a strip, for The marigold strips were also sampled during the example, once it may lead to important differences in period of onion cultivation, and each sample corre- species composition of a culture crop near or far from sponding to one square meter of crop coverage, us- the marigold strips. ing the same methodology as for onion plants. These The use of this plant may contribute to manage- marigold samples were taken randomly and at three ment of onion pests, mainly the thrips, because the in- developmental stages during the experiment: a) onset crease of the number of predators would promote low- flowering, when up to 10% of plants were flowering ering costs in pest control, thus, turning the organic (25 August and 7 September), plants were in full veg- onion crop more sustainable. Moreover, this study con- etative growth with few flowers (N = 8); b) peak flow- tributes to the identification of insect species occur- ering stage (N = 8), when more than 80% of the plants ring on both plants, providing basic information for were flowering (8 and 15 September); c) late flower- further researches. ing, when flowers were senescent and losing their at- The aim of this study was to determine the effect tractiveness (29 September and 6 October), and the of marigold plants near or far from organic onion cul- number of plants were lower, since they were dying tivation for maintenance of natural enemies, and study (N = 6). the arthropod composition and its abundance on on- The following ecological parameters were deter- ion and marigold fields. mined for onion and marigold using the software

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Biodiversity Pro® (McAleece, 1997): (i) Richness of account for more than 86% of the herbivores, was sig- species (the total number of species and morph spe- nificantly lower near the attractive plants. cies collected); abundance index (Lambshead et al., Another possible explanation for this result is that 1983), calculated from the mean of the entire 7-week marigold plants could produce repellent volatiles to sampling season of each species; (ii) Diversity index thrips, including T. tabaci. So, there would be less H’ (Shannon & Weaver, 1949), which considers the thrips near marigold strips because of its repellence, quantitative uniformity of each species in relation to not by natural enemy predation. As stated by Visser the others; (iii) Similarity index, calculated through (1986), phytophagous insects respond to a complex cluster analysis (Pielou, 1984), which indicates how mixture of plant odors to recognize their hosts. Four similar two substrates can be in relation to the spe- plant essential oils to repeal T. tabaci were tested by cies found. In this case the data were separated in two Tol et. al. (2007), who conclude that Origanum groups, phytophagous or entomophagous, and the majorana L. (Labiatae) is a promising thrips repellent whole sampling periods were considered for each sub- which could be used for further testing in a push–pull strate; and (iv) Correlation index (R2) (Sokal & Rohlf, system. Similar tests should be performed to identify 1969), which shows the dependence between two this possibility in relation to T. erecta. groups of data obtained from different plants. The analysis of ecological indices on grouped data Besides these indices, collection curves were cal- from onion (5 m and 30 m from the marigold strip, N culated for onion samples (Magurran, 1988). These = 70 for each) and marigold rows (N = 8 for onset curves may indicate whether sampling was regular and flowering stage and peak flowering stage and N = 6 enough to potentially collect all species that may be for late flowering stage) (Table 1) showed higher rich- present in the crop (for the whole experimental period, ness in samples near the marigold strip, with 37 taxa independently of the sampling week). or morphospecies, and 24 species in samples far from For the determination of these parameters, the marigold strip. The diversity index (H’) was higher arthropods presenting very low occurrence (one or at 5 m from the marigold strip, indicating that domi- two individuals) during the entire sampling period were nance of species is slightly lower than at 30 m from not included in analysis. the marigold strip. This is due to a higher number of T. tabaci individuals observed at 30 m than at 5 m RESULTS AND DISCUSSION from marigold. –2

First of all, the calculated collection curve indicated 120 that the 140 samples taken from onion crop were near from marigold – 5 m 100 P = 0.000009 enough to collect the majority of species present in the far from marigold – 30 m crop during the experiment. After the sampling 134 the 80 collection curve reaches the asymptotic position, in- 60 dicating that no new species were collected from this 40 point on. 20 Data from onion samples were taken at 5 m and 30 m from the marigold strip (Figure 1). Arthropods 0 Number of phytophagous arthropods m arthropods phytophagous of Number 8/25 9/1 9/8 9/15 9/22 9/29 10/6 were grouped in two main ecological groups: phytopha- Sample date gous and entomophagous, considering all specimens –2 5 found on samples, regardless of their higher or lower near from marigold – 5 m abundance. There was a higher number of phytopha- 4 gous arthopods m–2 in onion plants far from marigold far from marigold – 30 m (30 m). Despite the higher variation, the number of 3 -2 entomophagous arthopods m may explain this result, P = 0.000009 as the number of natural enemies was lower in plants 2 localized far from marigold row, therefore resulting in 1 higher amounts of herbivores. In this field there is a positive effect of marigold rows on natural enemy 0 abundance and negative effect on pest insect abun- m entomophagous of Number arthropods 8/25 9/1 9/8 9/15 9/22 9/29 10/6 Sample date dance. Similar results were reported by Driutti (1998) Figure 1 - Number of phytophagous and entomophagous using several plant species in surrounding rows and arthropods m–2 in an onion organic field with within organic onion fields, who found that the num- marigold rows at distances of 5 m (near) and 30 m ber of phytophagous insects, especially thrips, which (far).

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Table 1 - Average number of arthropods in each taxon collected/m2 sample, Richness, Abundance and Diversity (H’) in onion or marigold plants under organic farming.

Means/Sample1 Species/morphospecies - ecological niche oenion marigold flowering stag N)ear (5 m) Ftar (30 m oknse peea lat PHYTOPHAGOUS Thrips tabaci (4Thysanoptera: Thripidae) 292.5 335.2 0--.1 Therioaphis trifolii (Hemiptera: Aphidae) 2.94 3.36 3.13 - - L0athridiidae sp. (Insecta: Coleoptera) 09.8 03.1 08.1 0.8 Aphis fabae (Hemiptera: Aphidae) 0.33 1.11 11.63 4.75 1.17 schultzei (7Thysanoptera: Thripidae) 04.2 13.0 05.1 07.2 3.6 Haplothrips gowdeyii (Thysanoptera: Thripidae) 0.27 0.11 - 0.13 0.67 Caliothrips phaseoli (7Thysanoptera: Thripidae) 0-.0 -00.3 80.5 Neohydatotrhips sp. (Thysanoptera: Thripidae) 0.07 - 0.25 0.63 - Uroleucon ambrosiae (4Hemiptera: Aphidae) 0-.0 0--.2 5 Pseudodendrothrips sp. (Thysanoptera: Thripidae) 0.04 0.04 0.13 - - Lagria villosa (4Coleoptera: Lagriidae) 03.0 0-.0 0-.1 3 Acyrtosiphum kondoi (Hemiptera: Aphidae) 0.04 - 0.25 - - Taylorilygus pallidulus (3Hemiptera: Miridae) 06.0 0-.0 0-.1 3 Myzus persicae (Hemiptera: Aphidae) 0.03 0.03 0.25 0.13 0.33 Aphis s1p. (Hemiptera: Aphidae) 01.0 0---.4 Corytucha sp. (Hemiptera: Tingidae) 0.01 - - - 0.50 Creontidades rubrinervis (1Hemiptera: Miridae) 09.0 0---.1 Frankliniella insularis (Thysanoptera: Thripidae) 0.01 - - 0.25 - Neopamera bilobata (1Hemiptera: Lygaeidae) 0-.0 0--.1 3 Arorathrips sp. (Thysanoptera: Thripidae) - 0.09 - - 0.17 Macrosiphum euphorbiae (-3Hemiptera: Aphidae) 03.0 0-.6 Miridae sp2 (Insecta: Hemiptera) - 0.01 0.13 0.13 0.17 P--5syllidae sp1 (Insecta: Hemiptera) 0--.7 Psyllidae sp2 (Insecta: Hemiptera) - - - 0.5 0.33 M--0embracidae sp. (Insecta: Hemiptera) 0--.5 Lipaphis erysimi (Hemiptera: Aphidae) - - 0.50 - - Diabrotica speciosa (--8Coleoptera: Chrysomelidae) 08.3 0-.3 Aconophora sp. (Hemiptera: Membracidae) - - 0.25 - - Cerotoma arcuata (--3Coleoptera: Chrysomelidae) 03.1 0-.1 Liothrips sp1 (Thysanoptera: Phlaeothripidae) - - 0.13 - - M--3iridae sp3 (Insecta: Hemiptera) 03.1 0-.1 Sonesimia grossa (Hemiptera: Cicadellidae) - - 0.13 - - Frankliniella gemina (---8Thysanoptera: Thripidae) 43.3 23.3 Frankliniella rodeos (Thysanoptera: Thripidae) - - - 2.25 2.50 Frankliniella gardeniae (---5Thysanoptera: Thripidae) 03.2 18.3 Frankliniella sp1 (Thysanoptera: Thripidae) - - - 0.25 Harmostes s---5p1 (Hemiptera: Rhopalidae) 03.2 1.3 Acrosternum sp1 (Hemiptera: Pentatomidae) - - - 0.13 - M---3iridae sp1 (Insecta: Hemiptera) 0-.1 Nysius sp. (Hemiptera: Lygaeidae) - - - - 27.00

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Table 1 - Continuation. Frankliniella sp2 (Thysanoptera: Thripidae) - - - - 10.00 Frankliniella condei (----0Thysanoptera: Thripidae) 5.0 Utheteisa ornatrix (Lepidoptera: Arctiidae) - - - - 0.83 B----0ruchidae sp1 (Insecta: Coleoptera) 0.5 Paranapiacaba significata (Coleoptera: Chrysomelidae) - - - - 0.33 B----7ruchidae sp2 (Insecta: Coleoptera) 0.1 Curculionidae sp1 (Insecta: Coleoptera) - - - - 0.17 C----7urculionidae sp2 (Insecta: Coleoptera) 0.1 Miridae sp4 (Insecta: Hemiptera) - - - - 0.17 T6otal phytophagous/sample 297.5 471.9 270.0 146. 97.3 PREDATORS Stomatothrips angustipennis (1Thysan.: ) 01.2 0---. Stomatothrips rotundus (Thysan.: Aeolothripidae) 0.2 0.14 0.25 - Franklinothrips vespiformis (7Thysan.: Aeolothripidae) 04.0 0-3.0 0-.1 Orius insidiosus (Hemiptera: Anthocoridae) 0.07 - 5.38 4.88 10.83 T7homisidae (Araneae) 03.0 05.0 05.2 07.7 0.1 Nabis sp. (Hemiptera: Nabidae) 0.07 0.01 - 0.25 - C3occinellidae sp1 (Insecta: Coleoptera) 0-.0 - - Hippodamia convergens (Coleoptera: Coccinellidae) 0.03 - 0.13 0.25 - C1occinellidae sp2 (Insecta: Coleoptera) 0-.0 05.1 30-.2 Cycloneda sanguinea (Coleoptera: Coccinellidae) 0.01 0.09 0.13 - 0.50 Geocoris s1p. (Hemiptera: Lygaeidae) 0-.0 03.1 300.1 1.0 Scymnus sp. (Coleoptera: Coccinellidae) 0.01 - 0.25 0.63 2.00 S1taphylinidae sp2 (Insecta: Coleoptera) 0-.0 --70.1 Staphylinidae sp1 (Insecta: Coleoptera) - - 0.13 - - R--3eduviidae sp2 (Insecta: Hemiptera) 0--.1 Lebia sp1 (Coleoptera: Carabidae) - - - 0.25 - C---3occinellidae sp3 (Insecta: Coleoptera) 0-.1 Doru luteipes (Dermaptera: Forficulidae) - - - 0.13 - E---3lateridae sp1 (Insecta: Coleoptera) 0-.1 Reduviidae sp1 (Insecta: Hemiptera) - - - 0.13 - Orius perpunctatus (----7Hemiptera: Anthocoridae) 1.1 Misumenops pallidus (Araneae: Thomisidae) - - - - 0.17 Misumenops pallens (----7Araneae: Thomisidae) 0.1 Total predators/sample 0.8 0.41 6.91 8.04 16.18 PARASITOIDS Mymaridae sp2 (Insecta: Hymenoptera) 0.03 - - - - F3igitidae sp2 (Insecta: Hymenoptera) 0-.0 --70.1 Trichogrammatidae sp2 (Insecta: Hymenoptera) 0.03 - - - - M1ymaridae sp1 (Insecta: Hymenoptera) 01.0 0-5.0 07.2 0.1 Trichogrammatidae sp1 (Insecta: Hymenoptera) 0.01 0.01 - - - F-3igitidae sp1 (Insecta: Hymenoptera) 0---.0 Aprostocetus sp. (Hymenoptera: Eulophidae) - - 0.25 0.25 - Opius s--5p1 (Hymenoptera: Braconidae) 0--.2 sp (Insecta: Hymenoptera) - - 0.13 - 0.17 Continue...

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Table 1 - Continuation. Baryscapus sp1 (Hymenoptera: Eulophidae) - - 0.13 - - Galeopsomyia s--3p1 (Hymenoptera: Eulophidae) 0--.1 Lysiphlebus testaceipes (Hymenoptera: Braconidae) - - 0.13 - - M--3ymaridae sp3 (Insecta: Hymenoptera) 0--.1 Scelionidae sp4 (Insecta: Hymenoptera) - - 0.13 0.13 - T---5richogrammatidae sp3 (Insecta: Hymenoptera) 0-.2 Scelionidae sp1 (Insecta: Hymenoptera) - - - - 1.17 F----7igitidae sp3 (Insecta: Hymenoptera) 0.6 Scelionidae sp3 (Insecta: Hymenoptera) - - - - 0.50 S----7celionidae sp2 (Insecta: Hymenoptera) 0.1 Total parasitoids/sample 0.11 0.05 1.28 0.88 3.02 R7ichness 342040404 Total/sample 28.47 42.45 28.26 25.62 116.54 H3' 05.45 06.32 01.99 19.23 1.06 1Means/sample less than 0.03 in onion and marigold samples were disregarded.

In general, there was high similarity for the distance to marigold strip affect the values, since phythophagous (75.98 through cluster analysis, Table they were higher if compared onion at 5 m with on- 2) and correlation (R2 = 0.9985) between species col- ion at 30 m from the attractive plants. So these low lected in onions at 5 m and at 30 m from the mari- natural enemies’ similarities between marigold and on- gold strip, thus indicating high relation between the ion indicate that not the same but different species amount of each species in different distances. For were found on onion near attractive plants. Therefore, natural enemies these values are low (51.84% similar- the main phytophagous species were more abundant ity, Table 2, and R2 = 0.9063). In spite of these simi- in onion plants 30 m from marigold, while the main larities, the main phytophagous species collected, T. predators were more abundant in plants close to the tabaci, was 57% more abundant far from marigold attractive species. However, Gonçalves & Souza-Silva than near it. A similar result was found for the second (2003), studying only T. tabaci and Toxomerus spp. most abundant species, Therioaphis trifolii (Hemiptera: (Diptera: Syrphidae) populations in relation to differ- Aphidae), which was 15% more abundant far from the ent plant species in rows surrounding the onion field, marigold strip. The opposite was observed with preda- observed no population decrease of the pest species. tors, especially Stomatothrips angustipennis, This study, however, only included abundance of thrips Stomatothrips rotundus and Franklinothrips vespiformis nymphs and syrphid larvae, and there may have been (Thysanoptera: Aeolothripidae), which were twice as differences in the abundance of other phytophagous abundant in onion plants near the marigold strip. Para- and predatory species. sitoid abundance, in general, was very low in onion Higher herbivore species richness but lower abun- plants, but much lower far from the marigold strip dance were detected in plots near marigold than in plots (Table 1). Regarding marigold plants (Table 1) we far from marigold. Nineteen taxa 5 m from marigold found more richness and abundance of parasitoids com- and 15 taxa 30 m from onion plants were found. Phy- pared to onion plants, since those plants produce pol- tophagous insect abundance, however, was greater far len and nectar that potentially can sustain parasitoid from than near to marigold strips, 41.99 and 27.57 her- populations (Baggen, 1999). bivores / sample, respectively. Both greater abundance Very low percentages of similarity were observed and higher species richness of entomophagous species between phytophagous and entomophagous on onion (predators and parasitoids) were found in plots near compared to marigold (Table 2). For herbivores the marigold than in plots far from marigold. Eighteen taxa values are similar in relation to the distance from mari- 5 m from marigold and only ten 30 m from marigold gold, but become lower as the flowering stage ad- plants were found, as well as nearly twice as many vance. That was expected since the main herbivore natural enemies near to as far from marigold strips, species, T. tabaci, was not observed on marigold at 0.91 and 0.46 insects / sample, respectively. Hence, peak and late flowering stage. For natural enemies the we found higher diversity of both phytophagous and similarity was even lower compared to herbivores, but entomophagous species on onion plants close to mari-

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Table 2 - Cluster analysis (% similarity) for phytophagous and entomophagous among the different treatments for onion and marigold under organic farming. Pmhytophagous Otnion 30 Mkarigold - onse Mearigold - pea Marigold - lat Onion 5 m 75.9827 16.5648 8.4939 1.6795 O-3nion 30 m 155.282 64.223 3.645 Marigold - onset - - 34.6388 3.0578 Marigold - peak ---17.604 1 Entomophagous Onion 30 m Marigold - onset Marigold - peak Marigold - late O4nion 5 m 51.84 9.6322 76.7457 2.397 Onion 30 m - 3.934 2.0913 0.4386 M--4arigold - onset 677.485 46.185 Marigold - peak - - - 42.5552 gold rows, but increased herbivore abundance and de- of the phytophagous and 34% of the entire arthropod creased natural enemy abundance on onion plants at abundance at this stage. This tendency was confirmed greater distances from marigold. For the samples on at the end of the flowering period, when thrips abun- marigold strips, species dynamics varied depending on dance increased to 55% of the total arthropods. Be- the developmental stage, abundance and similarity sides these phytophagous species, the sucking hemi- (Tables 1 and 2), but not for richness: the same num- pteran Nysius sp. became very abundant in marigold ber of taxa (40) was collected considering all arthro- flowers at this stage. pod categories. While no numerical difference was This dominance of phytophagous taxa in the be- observed, species composition varied greatly between ginning and the end of marigold flowering periods, flowering stages. The analysis of similarity indices be- however, did not produce a great impact on the onion tween marigold developmental stages (Table 2) indi- field, because insects using marigold as a host plant cated that there is greater similarity between the onset (e.g. aphids, thrips or other phytophagous bugs) are and peak flowering periods for phytophagous (34.6%) not the same as those that attack onion plants, espe- than between the late flowering and the other stages cially T. tabaci, the primary onion pest (Table 1). This (3.05 to 17.6%). For the entomophagous the similari- is confirmed by the similarity index between onion and ties is bigger (Table 2) ranging between 42 and 67.5% marigold collections (Table 2), which reached 16.56% depending on the flowering stage. This indicates that between onion near marigold and the initial marigold a major number of natural enemy species uses the development stage. This is an indication that few phy- marigold strip during more time than the herbivores tophagous species were found at both plant species, do, witch is interesting for biological control. except for A. fabae and T. trifolli, which were col- The higher diversity index was observed in mari- lected in marigold and onion. gold during full bloom (H’, Table 1), when the preda- This study was set in a particular situation and tor Orius insidiosus was most abundant, as well as her- therefore the data would probably not fit the expecta- bivore Aphis fabae Scopoli (Hemiptera: Aphididae). tions of other people working on organic agriculture This is in accordance with previous observations. in other conditions. Thus, further tests could be nec- There was a slight dominance of phytophagous spe- essary to clarify the role of marigold plants near the cies at the beginning and at the end of flowering peri- onion crop in other areas. Anyway the data of the as- ods (the aphid A. fabae and the Lygaeidae Nysius sp., sociation of marigold plants and onion crops will cer- respectively), resulting in lower diversity indices at tainly help organic onion growers mainly in reducing these stages. The marigold at the onset of flowering the production costs. was more attractive to sucking phytophagous species, We found evidence that marigold strip is support- e.g. Hemiptera from the families Aphidae, Psyllidae and ing alternative prey and hosts, mainly from full blos- Membracidae, which combined represented over 60% som to the end of the flowering period, which are key of the collected individuals. This was expected because components of conservation biological control. This plants were still undergoing vegetative growth, i.e. fact is very important to maintain local populations of sprouting and producing flowers, which were attrac- generalist predators and parasitoids (Landis et al., tive to these species. At full flowering period, Aphidae 2000). For example, O. insidiosus abundance was represented only 29% of phytophagous species, when higher during late flowering, possibly in response to thrips (Thysanoptera) became dominant, with over 52% the increase in thrips number at that time. Since the

Sci. Agric. (Piracicaba, Braz.), v.66, n.6, p.780-787, November/December 2009 Natural enemies in onion fields 787 phytophagous species involved are not potential pests GONÇALVES, P.A.S.; SOUZA-SILVA, C.R. Efeito de espécies to onion plants, their population maintenance in the sys- vegetais em bordadura em cebola sobre a densidade populacional de tripes e sirfídeos predadores. Horticultura Brasileira, v.21, tem is not likely to have the associated negative im- p.731-734, 2003. pact of increasing crop herbivore. LANDIS, D.A.; WRATTEN, S.D.; GURR, G.M. Habitat management Therefore, keeping marigold rows close to the on- to conserve natural enemies of arthropod pests in agriculture. Annual Review of Entomology, v.45, p.175-201, 2000. ion field results in higher diversity and abundance of LAMBSHEAD, P.J.D.; PLATT, H.M.; SHAW K.M. Detection of natural enemies than when the attractive species is kept differences among assemblages of marine benthic species based far from onion plants. 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