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Natural parasitism of the coffee leaf miner: climate factors, insecticide, and landscape affecting parasitoid diversity and their ecosystem services in coffee agroecosystems

Published online by Cambridge University Press:  24 November 2023

Mateus P. dos Santos*
Affiliation:
Department of Plant Science and Animal Husbandry, State University of Southwestern Bahia, Vitória da Conquista, BA, Brazil
Benício de M. S. Neto
Affiliation:
Department of Plant Science and Animal Husbandry, State University of Southwestern Bahia, Vitória da Conquista, BA, Brazil
Ana C. P. Cardoso
Affiliation:
Department of Plant Science and Animal Husbandry, State University of Southwestern Bahia, Vitória da Conquista, BA, Brazil
Iuri dos Santos
Affiliation:
Department of Plant Science and Animal Husbandry, State University of Southwestern Bahia, Vitória da Conquista, BA, Brazil
Beatriz S. Coelho
Affiliation:
Department of Plant Science and Animal Husbandry, State University of Southwestern Bahia, Vitória da Conquista, BA, Brazil
Suzany A. Leite
Affiliation:
Department of Plant Science and Animal Husbandry, State University of Southwestern Bahia, Vitória da Conquista, BA, Brazil
Daniell R. R. Fernandes
Affiliation:
Coordination of Biodiversity – Sector of Entomology, National Research Institute, Manaus, Amazonas, Brazil
Geraldo A. Carvalho
Affiliation:
Departament of Entomology – Laboratory of Ecotoxicology and IPM, Federal University of Lavras, Lavras MG, Brazil
Maria A. Castellani
Affiliation:
Department of Plant Science and Animal Husbandry, State University of Southwestern Bahia, Vitória da Conquista, BA, Brazil
*
Corresponding author: Mateus P. dos Santos; Email: mateus.santos.0712@gmail.com

Abstract

Climate factors, pesticides, and landscape in coffee agroecosystems directly affect the populations of the coffee leaf miner and its parasitoids. This study aimed to investigate the effects of climate factors, insecticide use, and landscape on natural parasitism, parasitoid diversity, and infestation of L. coffeella in coffee plantations in the Planalto region, Bahia, Brazil. Mined leaves were collected monthly in six coffee plantations with varying edge density, vegetation cover, landscape diversity in scales of 500 to 3000 m of radius, insecticide use, and climate factors. Closterocerus coffeellae, and Proacrias coffeae (Eulophidae) predominated in the pest's natural parasitism. Our record is the first for the occurrence of Stiropius reticulatus, Neochrysocharis sp. 1, Neochrysocharis sp. 2, and Zagrammosoma sp. in Bahia. Higher temperature and larger forest cover increased the coffee leaf miner infestation. Higher rainfall values, insecticide use, and landscape diversity decreased the pest infestations. Natural parasitism and species diversity are favoured by increase in temperature, forest cover, and edge density, while increase in rainfall, insecticide use, and landscape diversity lead them to decrease.The natural parasitism and diversity of parasitoid species of the coffee leaf miner have been enhancing in the areas with greater forest cover and edge density associated with low use of insecticides. The areas composed of different lands with annual croplands surrounding the coffee plantations showed less natural parasitism and parasitoid species diversity. The ecosystem services provided by C. coffeellae and P. coffeae in coffee crops areas require conservation and these species are potential bioproducts for applied biological control programmes.

Type
Research Paper
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press

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References

Allinne, C, Savary, S and Avelino, J (2016) Delicate balance between pest and disease injuries, yield performance, and other ecosystem services in the complex coffee-based systems of Costa Rica. Agriculture, Ecosystems & Environment 222, 112.CrossRefGoogle Scholar
Amaral, DS, Venzon, M, Pallini, A, Lima, PC and De Souza, O (2010) A diversificação da vegetação reduz o ataque do bicho-mineiro-do-cafeeiro Leucoptera coffeella (Guérin-mèneville) (Lepidoptera: Lyonetiidae)? Neotropical Entomology 39, 543548.CrossRefGoogle ScholarPubMed
Aristizábal, N and Metzger, JP (2019) Landscape structure regulates pest control provided by ants in sun coffee farms. Journal of Applied Ecology 56, 2130.CrossRefGoogle Scholar
Bacca, T, Lima, ER, Picanço, MC, Guedes, RNC and Viana, JHM (2006) Optimum spacing of pheromone traps for monitoring the coffee leaf miner Leucoptera coffeella. Entomologia Experimentalis et Applicata 119, 3945.CrossRefGoogle Scholar
Bacci, L, Fernandes, F, Picanço, M, Crespo, A and Campos, M (2006) Seletividade fisiológica de inseticidas a vespas predadoras (Hymenoptera: Vespidae) de Leucoptera coffeella (Lepidoptera: Lyonetiidae). BioAssay 1, 17. doi: 10.14295/BA.v1.0.38Google Scholar
Bakker, L, Van der Werf, W and Bianchi, FJJA (2021) No significant effects of insecticide use indicators and landscape variables on biocontrol in field margins. Agriculture, Ecosystems & Environment 308, 107253.CrossRefGoogle Scholar
Basha, HA, Mostafa, EM and Eldeeb, AM (2021) Mite pests and their predators on seven vegetable crops (Arachnida: Acari). Saudi Journal of Biological Sciences 28, 34143417.CrossRefGoogle ScholarPubMed
Bates, D, Mächler, M, Bolker, B and Walker, S (2015) R package. Fitting linear mixed-effects models using lme4. arXiv preprint arXiv:1406.5823, 114. doi: 10.18637/jss.v067.i01Google Scholar
Bolker, B and Team R (2010) bbmle: Tools for general maximum likelihood estimation. R package.Google Scholar
Burnham, KP and Anderson, DR (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociological Methods & Research 33, 261304.CrossRefGoogle Scholar
Calderón-Arroyo, C, Togni, PHB, Pantoja, GM, Saenz, AS and Venzon, M (2023) Plants for fitness enhancement of a coffee leaf miner parasitoid. Agriculture 13, 244.CrossRefGoogle Scholar
Carvalho, GA, Miranda, JC, Vilela, FZ, Moura, AP and Moraes, JC (2004) Impacto de inseticidas sobre vespas predadoras e parasitóides e sua eficiência no controle de Leucoptera coffeella (Guérin-Mèneville & Perrottet, 1842) (Lepidoptera: Lyonetiidae). Arquivos do Instituto Biológico 71, 6370.Google Scholar
Carvalho, GA, Miranda, JC, Moura, AP, Rocha, LCD, Reis, PR and Vilela, FZ (2005) Controle de Leucoptera coffeella (Guérin-Mèneville & Perrottet, 1842) (Lepidoptera: Lyonetiidae) com inseticidas granulados e seus efeitos sobre vespas predadoras e parasitóides. Arquivos do Instituto Biológico 72, 6372.CrossRefGoogle Scholar
Carvalho, GA, Grützmacher, AD, Passos, LC and Oliveira, RL (2019) Physiological and ecological selectivity of pesticides for natural enemies of insects. In Souza, B, Vázquez, L and Marucci, R (eds), Natural Enemies of Insect Pests in Neotropical Agroecosystems: Biological Control and Functional Biodiversity. New York: Springer, pp. 469478.CrossRefGoogle Scholar
Companhia Nacional de Abastecimento (CONAB) (2022) Acompanhamento da safra brasileira de café – safra 2022. 9(3), 66.Google Scholar
Costa, DP, Fernandes, FL, Alves, FM, da Silva, ÉM and Visôtto, LE (2016) Resistance to insecticides in populations of the coffee leafminer. In Trdan, S (ed.), Insecticides Resistance: BoD–Books on Demand. Croatia: InTech, pp. 317. doi: 10.5772/60478Google Scholar
Custódio, AADP, Moraes, JC, Custódio, AADP, Lima, LA, Faria, MAD and Gomes, NM (2009) Incidência do bicho-mineiro do cafeeiro em lavoura irrigada sob pivô central. Coffee Science 4, 1626.Google Scholar
Dantas, J, Motta, IO, Vidal, LA, Nascimento, EFMB, Bilio, J, Pupe, JM, Veiga, A, Carvalho, C, Lopes, RB, Rocha, TL, Silva, LP, Pujol-Luz, JR and Albuquerque, ÉVS (2021) A comprehensive review of the coffee leaf miner Leucoptera coffeella (Lepidoptera: Lyonetiidae) – a major pest for the coffee crop in Brazil and others neotropical countries. Insects 12, 1130.CrossRefGoogle Scholar
David-Rueda, G, Constantino, LM, Cecilia Montoya, E, Ortega, OE, Nancy Gil, Z and Benavides-Machado, P (2016) Diagnostic of Leucoptera coffeella (Lepidoptera: Lyonetiidae) and its parasitoids in the department of Antioquia, Colombia. Revista Colombiana de Entomología 42, 411.CrossRefGoogle Scholar
De la Mora, A, García-Ballinas, JA and Philpott, SM (2015) Local, landscape, and diversity drivers of predation services provided by ants in a coffee landscape in Chiapas, Mexico. Agriculture, Ecosystems & Environment 201, 8391.CrossRefGoogle Scholar
Ecole, CC, Moraes, JC and Vilela, M (2010) Suplementos alimentares e isca tóxica no manejo do bicho-mineiro e de seus inimigos naturais. Coffee Science 5, 167172.Google Scholar
Fernandes, FL, Mantovani, EC, Bonfim Neto, H and Nunes, VDV (2009) Efeitos de variáveis ambientais, irrigação e vespas predadoras sobre Leucoptera coffeella (Guérin-Méneville) (Lepidoptera: Lyonetiidae) no cafeeiro. Neotropical Entomology 38, 410417.CrossRefGoogle Scholar
Fernandes, FL, Silva, PR, Gorri, JER, Pucci, LF and Silva, ÍW (2014) Selectivity of old and new insecticides and behaviour of vespidae predators in coffee crop. Sociobiology 60, 471476.CrossRefGoogle Scholar
Fragoso, DB, Jusselino-Filho, P, Guedes, RN and Proque, R (2001) Seletividade de inseticidas a vespas predadoras de Leucoptera coffeella (Guér-Mènev.) (Lepidoptera: Lyonetiidae). Neotropical Entomology 30, 139143.CrossRefGoogle Scholar
Fragoso, DB, Guedes, RNC, Picanço, MC and Zambolim, L (2002) Insecticide use and organophosphate resistance in the coffee leaf miner Leucoptera coffeella (Lepidoptera: Lyonetiidae). Bullettin of Entomology Research 92, 203212.CrossRefGoogle ScholarPubMed
Gravena, S (1983) Táticas de manejo integrado do bicho mineiro do cafeeiro Perileucoptera coffeella (Guérin-Méneville, 1842): I-Dinâmica populacional e inimigos naturais. Anais da Sociedade Entomológica do Brasil 12, 6171. doi: 10.37486/0301-8059.v12i1.300CrossRefGoogle Scholar
Gravesen, L (2003) The treatment frequency index: an indicator for pesticide use and dependency as well as overall load on the environment. In: Reducing pesticide dependency in Europe to protect health, environment and biodiversity, Copenhagen, Pesticides Action Network Europe (PAN), Pure Conference.Google Scholar
Gusmão, MR, Picanço, M, Gonring, AHR and Moura, MF (2000) Seletividade fisiológica de inseticidas a Vespidae predadores do bicho-mineiro-do-cafeeiro. Pesquisa Agropecuária Brasileira 35, 681686.CrossRefGoogle Scholar
Harelimana, A, Rukazambuga, D and Hance, T (2022) Pests and diseases regulation in coffee agroecosystems by management systems and resistance in changing climate conditions: a review. Journal of Plant Diseases and Protection 129, 10411052.CrossRefGoogle Scholar
Hohlenwerger, C, Tambosi, LR and Metzger, JP (2022) Forest cover and proximity to forest affect predation by natural enemies in pasture and coffee plantations differently. Agriculture, Ecosystems & Environment 333, 107958.CrossRefGoogle Scholar
Ihering, RV (1914) Três Chalcididas parasitas do Bicho do café, Leucoptera coffeella, com algumas consideraçoes sobre o hyperparasitismo. Revista do Museu Paulista 9, 85106.Google Scholar
Instituto Nacional de Pesquisas Espaciais (INPE) (2022 a) Sistema Integrado de Dados Ambientais. Available at http://sinda.crn.inpe.br/PCD/SITE/novo/site/index.php (Access on 5 june 2022).Google Scholar
Instituto Nacional de Pesquisas Espaciais (INPE) (2022 b) Câmeras Imageadoras CBERS 04A. Available at http://www.cbers.inpe.br/sobre/cameras/cbers04a.php (Access on 07 may 2022).Google Scholar
Iverson, AL, Gonthier, DJ, Pak, D, Ennis, KK, Burnham, RJ, Perfecto, I, Rodriguez, MR and Vandermeer, JH (2019) A multifunctional approach for achieving simultaneous biodiversity conservation and farmer livelihood in coffee agroecosystems. Biological Conservation 238, 108179.CrossRefGoogle Scholar
Jaramillo, MG, Garcia-Gonzalez, J and Rugno, JB (2019) Fertility life table of Leucoptera coffeella (Guérin-Mèneville) (Lepidoptera: Lyonetiidae) at seven temperatures in coffee. American Journal of Entomology 3, 7076.CrossRefGoogle Scholar
Krebs, CJ (2014) Community Structure in Space: Biodiversity. In Krebs, CJ (ed.), Ecology: The Experimental Analysis of Distribution and Abundance, Sixth Edition, Edinburgh: Pearson Benjamin Cummings, pp. 363387.Google Scholar
Leite, SA, Dos Santos, MP, Resende-Silva, GA, da Costa, DR, Moreira, AA, Lemos, OL, Guedes, RNC and Castellani, MA (2020 a) Area-wide survey of chlorantraniliprole resistance and control failure likelihood of the Neotropical coffee leaf miner Leucoptera coffeella (Lepidoptera: Lyonetiidae). Journal of Economic Entomology 113, 13991410.CrossRefGoogle ScholarPubMed
Leite, SA, Guedes, RNC, Santos, MP, Costa, DR, Moreira, AA, Matsumoto, SN, Lemos, OL and Castellani, MA (2020 b) Profile of coffee crops and management of the neotropical coffee leaf miner, Leucoptera coffeella. Sustainability 12, 8011.CrossRefGoogle Scholar
Leite, SA, dos Santos, MP, da Costa, DR, Moreira, AA, Guedes, RNC and Castellani, MA (2021) Time-concentration interplay in insecticide resistance among populations of the Neotropical coffee leaf miner, Leucoptera coffeella. Agricultural and Forest Entomology 23, 232241.CrossRefGoogle Scholar
Leite, SA, Guedes, RNC, da Costa, DR, Colmenarez, YC, Matsumoto, SN, Dos Santos, MP, Coelho, BS, Moreira, AA and Castellani, MA (2022) The effects of thiamethoxam on coffee seedling morphophysiology and Neotropical leaf miner (Leucoptera coffeella) infestations. Pest Management Science 78, 25812587.CrossRefGoogle ScholarPubMed
Lenth, RV (2020) emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.4.5. Available at https://CRAN.R-project.org/package=emmeans (Acessado em: 10 de maio de 2021).Google Scholar
Librán-Embid, F, De Coster, G and Metzger, JP (2017) Effects of bird and bat exclusion on coffee pest control at multiple spatial scales. Landscape Ecology 32, 19071920.CrossRefGoogle Scholar
Lomelí-Flores, JR, Barrera, JF and Bernal, JS (2009) Impact of natural enemies on coffee leafminer Leucoptera coffeella (Lepidoptera: Lyonetiidae) population dynamics in Chiapas, Mexico. Biological Control 51, 5160.CrossRefGoogle Scholar
Lomelí-Flores, JR, Barrera, JF and Bernal, JS (2010) Impacts of weather, shade cover and elevation on coffee leafminer Leucoptera coffeella (Lepidoptera: Lyonetiidae) population dynamics and natural enemies. Crop Protection 29, 10391048.CrossRefGoogle Scholar
Marques, KBSC, Fernandes, LG, Morais, LC, Haddi, K and Silveira, LCP (2022) Diversity of hymenopteran parasitoids in coffee plantations under agroecological transition and its impact on coffee leaf miner (Leucoptera coffeella) infestations. Diversity 15, 2.CrossRefGoogle Scholar
McGarigal, K and Marks, B (1995) FRAGSTATS: Spatial Analysis Program for Quantifying Landscape Structure. USDA Forest Service Gen. Tech. Rep. PNW-GTR-351. Portland, OR: U.S. Department of Agriculture, Forest Service, Pacific Northwest Research Station.Google Scholar
Medeiros, HR, Grandinete, YC, Manning, P, Harper, KA, Cutler, GC, Tyedmers, P, Righi, CA and Ribeiro, MC (2019 a) Forest cover enhances natural enemy diversity and biological control services in Brazilian sun coffee plantations. Agronomy for Sustainable Development 39, 19.CrossRefGoogle Scholar
Medeiros, HR, Martello, F, Almeida, EA, Mengual, X, Harper, KA, Grandinete, YC, Metzger, JP, Righi, CA and Ribeiro, MC (2019 b) Landscape structure shapes the diversity of beneficial insects in coffee producing landscapes. Biological Conservation 238, 108193.CrossRefGoogle Scholar
Melo, TL (2005) Flutuação populacional, predação e parasitismo do bicho-mineiro Leucoptera coffeella (Guérin-Mèneville e Perrotet, 1842) (Lepidoptera: Lyonetiidae) em duas regiões cafeeiras do Estado da Bahia. Master Thesis, Universidade Estadual do Sudoeste da Bahia, Vitória da Conquista, Bahia, Brasil.Google Scholar
Melo, TL, Castellani, MA, Nascimento, MDLD, Menezes Junior, ADO, Ferreira, GFP and Lemos, OL (2007) Comunidades de parasitóides de Leucoptera coffeella (Guérin-Mèneville & Perrottet, 1842) (Lepidoptera: Lyonetiidae) em cafeeiros nas regiões Oeste e Sudoeste da Bahia. Ciência e Agrotecnologia 31, 966972.CrossRefGoogle Scholar
Melo, TL, Raetano, CG, Nery, MS, Cardoso, AD, Moreira, AA, Leite, SA, Jesus, TF, Silva, WGO and Castellani, MA (2019) Management of coffee leaf miner: spray volume, efficacy of cartap hydrochloride and impact on parasitism. Coffee Science 14, 250260.CrossRefGoogle Scholar
Morgan, WH, Thébault, E, Seymour, CL and Van Veen, FF (2017) Density dependence and environmental factors affect population stability of an agricultural pest and its specialist parasitoid. BioControl 62, 175184.CrossRefGoogle Scholar
Nestel, D, Dickschen, F and Altieri, MA (1994) Seasonal and spatial population loads of a tropical insect: the case of the coffee leaf-miner in Mexico. Ecological Entomology 19, 159167.CrossRefGoogle Scholar
Pantoja-Gomez, LM, Corrêa, AS, de Oliveira, LO and Guedes, RNC (2019) Common origin of Brazilian and Colombian populations of the neotropical coffee leaf miner, Leucoptera coffeella (Lepidoptera: Lyonetiidae). Journal of Economic Entomology 112, 924931.CrossRefGoogle ScholarPubMed
Parra, JRP and Reis, PR (2013) Manejo integrado para as principais pragas da cafeicultura, no Brasil. Visão Agrícola 8, 4750.Google Scholar
Parra, JRP, Gonçalves, W, Gravena, S and Marconato, AR (1977) Parasitos e predadores do bicho-mineiro do cafeeiro Perileucoptera coffeella (Guérin-Méneville, 1842) em São Paulo. Anais da Sociedade Entomológica do Brasil 6, 138143.CrossRefGoogle Scholar
Penteado-Dias, AM (1999) New species of parasitoids on Perileucoptera coffeella (Guérin-Menèville) (Lepidoptera, Lyonetiidae) from Brazil. Zoologische Mededelingen 73, 189197.Google Scholar
Pereira, EJG, Picanço, MC, Bacci, L, Della Lucia, TMC, Silva, ÉM and Fernandes, FL (2007 a) Natural mortality factors of Leucoptera coffeella (Lepidoptera: Lyonetiidae) on Coffea arabica. Biocontrol Science and Technology 17, 441455.CrossRefGoogle Scholar
Pereira, EJG, Picanço, MC, Bacci, L, Crespo, ALB and Guedes, RNC (2007 b) Seasonal mortality factors of the coffee leafminer, Leucoptera coffeella. Bulletin of Entomological Research 97, 421432.CrossRefGoogle ScholarPubMed
Perfecto, I, Vandermeer, J and Philpott, SM (2010) Complejidad ecológica y el control de plagas en un cafetal orgánico: develando un servicio ecosistémico autónomo. Agroecología 5, 4151.Google Scholar
Picanço, MC, Oliveira, IR, Fernandes, FL, Martinez, HEP, Bacci, L and Silva, EM (2012) Ecology of Vespidae (Hymenoptera) predators in Coffea arabica plantations. Sociobiology 59, 12691280.Google Scholar
R Development Core Team (2020) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. Available at http://www.R-project.org.Google Scholar
Reis, PR and Souza, JD (1996) Manejo integrado do bicho-mineiro, Perileucoptera coffeella (Guérin-Meneville) (Lepidoptera: Lyonetiidae), e seu reflexo na produção de café. Anais da Sociedade Entomológica do Brasil 25, 7782.CrossRefGoogle Scholar
Reis, R Jr., Souza, OD and Vilela, EF (2000) Predators impairing the natural biological control of parasitoids. Anais da Sociedade Entomológica do Brasil 29, 507514.CrossRefGoogle Scholar
Rempel, RS, Kaukinen, D and Carr, AP (2012) Patch Analyst 5.1: Ontario Ministry of Natural Resources. Thunder Bay, ON: Centre for Northern Forest Ecosystem Research.Google Scholar
Rezende, MQ, Venzon, M, Perez, AL, Cardoso, IM and Janssen, A (2014) Extrafloral nectaries of associated trees can enhance natural pest control. Agriculture, Ecosystems & Environment 188, 198203.CrossRefGoogle Scholar
Rezende, MQ, Venzon, M, Santos, PS, Cardoso, IM and Janssen, A (2021) Extrafloral nectary-bearing leguminous trees enhance pest control and increase fruit weight in associated coffee plants. Agriculture, Ecosystems & Environment 319, 107538. doi: 10.1016/j.agee.2021.107538CrossRefGoogle Scholar
Righi, CA, Campoe, OC, Bernardes, MS, Lunz, AMP, Piedade, SMS and Pereira, CR (2013) Influence of rubber trees on leaf-miner damage to coffee plants in an agroforestry system. Agroforestry Systems 87, 13511362.CrossRefGoogle Scholar
Rocha, ÉAA, Silva, RM, da Silva, BKR, Cruz, CG and Fernandes, FL (2022) Fitness cost and reversion of resistance Leucoptera coffeella (Lepidoptera: Lyonetiidae) to chlorpyrifos. Ecotoxicology and Environmental Safety 242, 113831.CrossRefGoogle Scholar
Rosado, MC, Araújo, GJ, Pallini, A and Venzon, M (2021) Cover crop intercropping increases biological control in coffee crops. Biological Control 160, 104675.CrossRefGoogle Scholar
SAS Institute (2011) SAS/STAT User's Guide, Release 9.0. Cary: SAS Institute.Google Scholar
Schauff, ME, LaSalle, J and Coote, LD (1997) Eulophidae. In Gibson, GAP, Huber, JT and Woolley, JB (eds), Annotated Keys to the Genera of Nearctic Chalcidoidea (Hymenoptera). Ottawa: NRC Rearch Press, pp. 327429.Google Scholar
Souza, JC and Reis, PR (2000) Pragas do cafeeiro – reconhecimento e controle. Viçosa: CTP, 154p.Google Scholar
Stüber, M, Tack, AJ, Zewdie, B, Mendesil, E, Shimales, T, Ayalew, B, Nemomissa, S, Sjögren, J, Vesterinen, E, Wezel, A and Hylander, K (2021) Multi-scale mosaics in top-down pest control by ants from natural coffee forests to plantations. Ecology 102, e03376.CrossRefGoogle ScholarPubMed
Superintendência de Estudos Econômicos e Sociais da Bahia (SEI) (1998) Informações municipais. Disponível em. Available at https://www.sei.ba.gov.br/index.php?option=com_wrapper&view=wrapper&Itemid=266 (Acesso em 01 maio de 2022).Google Scholar
Superintendência de Estudos Econômicos e Sociais da Bahia (SEI) (2015) Sistemas de Informações Municipais. Disponível em. Available at http://sim.sei.ba.gov.br/sim/tabelas.wsp# (Acesso em 01 maio de 2022).Google Scholar
Tango, MF, Fernandes, DR, Paz, CC, Lara, RI and Perioto, NW (2014) Orgilinae (Hymenoptera: Braconidae) in coffee crops at Cravinhos, State of São Paulo, Brazil. Revista Colombiana de Entomología 40, 2533.Google Scholar
Tomazella, VB, Jacques, GC, Lira, AC and Silveira, LCP (2018) Visitation of social wasps in arabica coffee crop (Coffea arabica L.) intercropped with different tree species. Sociobiology 65, 299304.CrossRefGoogle Scholar
Tuelher, ES, de Oliveira, EE, Guedes, RNC and Magalhães, LC (2003) Ocorrência de bicho-mineiro do cafeeiro (Leucoptera coffeella) influenciada pelo período estacional e pela altitude. Acta Scientiarum. Agronomy 25, 119124.Google Scholar
Vandermeer, J, Perfecto, I and Schellhorn, N (2010) Propagating sinks, ephemeral sources and percolating mosaics: conservation in landscapes. Landscape Ecology 25, 509518.CrossRefGoogle Scholar
Vega, FE, Posada, F and Infante, F (2007) Coffee insects: ecology and control. In Pimentel, D (ed.), Encyclopedia of Pest Management, Vol. II. New York: CRC Press Taylor & Francis Group, pp. 9598.Google Scholar
Venzon, M (2021) Agro-ecological management of coffee pests in Brazil. Frontiers in Sustainable Food Systems 323, 113. doi: 10.3389/fsufs.2021.721117Google Scholar
Vilchez-Mendoza, S, Romero-Gurdián, A, Avelino, J, DeClerck, F, Bommel, P, Betbeder, J, Cilas, C and Beilhe, LB (2022) Assessing the joint effects of landscape, farm features and crop management practices on berry damage in coffee plantations. Agriculture, Ecosystems & Environment 330, 107903.CrossRefGoogle Scholar
Villa, M, Santos, SA, Sousa, JP, Ferreira, A, da Silva, PM, Patanita, I, Ortega, M, Pascual, S and Pereira, JA (2020) Landscape composition and configuration affect the abundance of the olive moth (Prays oleae, Bernard) in olive groves. Agriculture, Ecosystems & Environment 294, 106854.CrossRefGoogle Scholar
Wharton, RA, Marsh, PM and Sharkey, MJ (eds) (1997) Manual of the New World Genera of the Family Braconidae (Hymenoptera). Washington: Special Publication of the International Society of Hymenopterists, N° 1, 439p.Google Scholar
Zuur, AF, Ieno, EN, Walker, NJ, Saveliev, AA and Smith, GM (2009) Mixed Effects Models and Extensions in Ecology with R. Vol. 574. New York: Springer.CrossRefGoogle Scholar
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