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Effect of pigeon pea intercropping or shading with leucaena plants on the occurrence of the coffee leaf miner and on its predation by wasps in organic coffee plantings

Efeito da consorciação com feijão-guandu ou sombreamento com plantas de leucena na ocorrência do Bicho-mineiro e sua predação por vespas em lavouras de café orgânico

ABSTRACT:

The infestation of coffee leaf miner and its predation by wasps were assessed in commercial organic coffee plantings shaded with leucaena or intercropped with pigeon pea. Plantings in northern Paraná were assessed every two weeks from June 2011 to December 2012. The percent of infested leaves, number of mines per leaf and the percent of predation by wasps (indicated by lacerations) were determined. Fewer coffee leaf miners and fewer mines per leaf were found in pigeon pea intercropped plantings (28.4% and 0.3, respectively) than in shaded plantings with leucaena (48.1% and 0.8, respectively). More predation by wasps was found in the shaded (27.2%) than in the intercropped (13.2%) plantings. Suggestions for new studies are presented along with suggestions for managing the leaf miner in coffee plantings.

Key words:
Leucoptera coffeella; coffee pests; organic farming; biological control

RESUMO:

A infestação de bicho-mineiro e a sua predação por vespas foram avaliadas em lavouras comerciais de café orgânico sombreadas com leucena ou consorciadas com feijão guandu. As lavouras situadas na região Norte do Paraná foram avaliadas a cada duas semanas de junho de 2011 a dezembro de 2012. Determinou-se o percentual de folhas infestadas, o número de minas por folha e a porcentagem de predação por vespas (indicada pela laceração das minas). Menor infestação do Bicho-mineiro e o menor número de minas por folha foi verificada na lavoura consorciada com feijão guandu (28,4% e 0,3; respectivamente) em relação a lavoura sombreada com leucina (48,1% e 0,8; respectivamente). Maior predação por vespas foi verificada na lavoura sombreada (27,2%) em relação a lavoura consorciada (13,18%). Sugestões de novas pesquisas e para o manejo do bicho-mineiro em lavouras de café são apresentadas.

Palavras-chave:
Leucoptera coffeella; pragas do café; cultivo orgânico; controle biológico

INTRODUCTION:

The coffee leaf miner (CLM) Leucoptera coffeella (Lepidoptera: Lyonetiidae) is one of the key pests of coffee plantings and is reported in coffee growing regions throughout the world (PEREIRA et al., 2007PEREIRA, E.J.G. et al. Seasonal mortality factors of the coffee leaf miner, Leucoptera coffeella. Bulletin of Entomological Research, Cambridge, v.97, n.4, p.421-432, 2007. Available from: https://doi.org/10.1017/S0007485307005202>. Accessed: Aug. 27, 2016. doi: 10.1017/S0007485307005202.
https://doi.org/10.1017/S000748530700520...
; SCALÓN et al., 2011SCALÓN, J.D. et al. Spatial and temporal dynamics of coffee-leaf-miner and predatory wasps in organic coffee field in formation. Ciência Rural, Santa Maria, v.41, n.4, p.646-652, 2011. Available from: http://dx.doi.org/10.1590/S0103-84782011005000037>. Accessed: Aug. 27, 2016. doi: 10.1590/S0103-84782011005000037.
http://dx.doi.org/10.1590/S0103-84782011...
; RIGHI et al., 2013RIGHI, C.A. et al. Influence of rubber trees on leaf-miner damage to coffee plants in an agroforestry system. Agroforestry Systems, v.87, n.6, p.1351-1362, 2013. Available from: https://doi.org/10.1007/s10457-013-9642-9>. Accessed: Aug. 27, 2016. doi: 10.1007/s10457-013-9642-9.
https://doi.org/10.1007/s10457-013-9642-...
). The CLM larva mines the palisade parenchyma, prevents photosynthesis (NEVES et al., 2006NEVES, A.D. et al. A new concept for insect damage evaluation based on plant physiological variables. Anais da Academia Brasileira de Ciências, Rio de Janeiro, v.78, n.4, p.821-835, 2006. Available from: http://dx.doi.org/10.1590/S0001-37652006000400015>. Accessed: Aug. 27, 2016. doi: 10.1590/S0001-37652006000400015.
http://dx.doi.org/10.1590/S0001-37652006...
), and may result in yield losses of 50% if control measures are not adopted (REIS & SOUZA, 1996REIS, P.R.; SOUZA, J.C. Manejo integrado do bicho-mineiro, Perileucoptera coffeella (Guérin-Mèneville) (Lepidoptera: Lyonetiidae), e seu reflexo na produção de café. Anais da Sociedade Entomológica do Brasil, v.25, n.1, p.77-82, 1996.).

In conventional farming systems, synthetic chemical insecticides are ordinarily used. However, chemical insecticides may fail to control the target pests and can sometimes fostering other pests (CORDEIRO et al., 2013CORDEIRO, E.M.G. et al. Beyond selectivity: Are behavioral avoidance and hormesis likely causes of pyrethroid-induced outbreaks of the southern red mite Oligonychus ilicis? Chemosphere, Amsterdam, v.93, n.6, p.1111-1116, 2013. Available from: https://doi.org/10.1016/j.chemosphere.2013.06.030>. Accessed: Aug. 27, 2016. doi: 10.1016/j.chemosphere.2013.06.030.
https://doi.org/10.1016/j.chemosphere.20...
). For example, CLM populations resistant to insecticides have been observed under field conditions (FRAGOSO et al., 2003FRAGOSO, D.B. et al. Selection in the evolution of resistance to organophosphates in Leucoptera coffeella (Guérin-Mèneville) (Lepidoptera: Lyonetiidae). Neotropical Entomology , Londrina, v.32, n.2, p.329-334, 2003. Available from: http://dx.doi.org/10.1590/S1519-566X2003000200020>. Accessed: Aug. 27, 2016. doi: 10.1590/S1519-566X2003000200020.
http://dx.doi.org/10.1590/S1519-566X2003...
; RIBEIRO et al., 2003RIBEIRO, B.M. et al. Níveis de resistência a inseticidas organo-fosforados em populações de Leucoptera coffeella (Guèr-Ménev) (Lepidoptera: Lyonetiidae) de Minas Gerais. Bioscience Journal, Uberlândia, v.19, n.2, p.73-77, 2003. Available from: http://www.seer.ufu.br/index.php/biosciencejournal/article/viewFile/6455/4189>. Accessed: Aug. 27, 2016.
http://www.seer.ufu.br/index.php/bioscie...
). Furthermore, secondary pest outbreaks, mostly of the red mite Oligonychus ilicis McGregor (Acari: Tetranychidae), have also been reported after spraying of pyrethroid insecticides (COREDEIRO et al., 2013). Moreover, many insecticides used to control CLM have resulted in the death of predatory wasps or at least reduced wasp activity (FERNANDES et al., 2013FERNANDES, F.L. et al. Selectivity of Old and New Organophosphate Insecticides and Behaviour of Vespidae Predators in Coffee Crop. Sociobiology, Feira de Santana, v.60, n.4, p.471-476, 2013. Available from: http://dx.doi.org/10.13102/sociobiology.v60i4.471-476>. Accessed: Aug. 29, 2017. doi: 10.13102/sociobiology.v60i4.471-476.
http://dx.doi.org/10.13102/sociobiology....
), resulting in losses to the coffee agroecosystem, in which wasps are important natural enemies of CLM (TUELHER et al., 2003TUELHER, E.S. et al. Occurrence of coffee leaf-miner (Leucoptera coffeella) influenced by season and altitude. Acta Scientiarum: Agronomy, Maringá, v.25, n.1, p.119-124, 2003. Available from: http://dx.doi.org/10.4025/actasciagron.v25i1.2458>. Accessed: Aug. 29, 2017. doi: 10.4025/actasciagron.v25i1.2458.
http://dx.doi.org/10.4025/actasciagron.v...
; PEREIRA et al., 2007PEREIRA, E.J.G. et al. Seasonal mortality factors of the coffee leaf miner, Leucoptera coffeella. Bulletin of Entomological Research, Cambridge, v.97, n.4, p.421-432, 2007. Available from: https://doi.org/10.1017/S0007485307005202>. Accessed: Aug. 27, 2016. doi: 10.1017/S0007485307005202.
https://doi.org/10.1017/S000748530700520...
; SCALÓN et al., 2011SCALÓN, J.D. et al. Spatial and temporal dynamics of coffee-leaf-miner and predatory wasps in organic coffee field in formation. Ciência Rural, Santa Maria, v.41, n.4, p.646-652, 2011. Available from: http://dx.doi.org/10.1590/S0103-84782011005000037>. Accessed: Aug. 27, 2016. doi: 10.1590/S0103-84782011005000037.
http://dx.doi.org/10.1590/S0103-84782011...
).

The search for cropping systems that avoid the use of insecticides is desirable, and in this sense, the improvement of biodiversity could possibly serve to enhance agroecosystem resilience and reduce insect pests in field crops and forests (GURR et al., 2003GURR, G.M. et al. Multi-function agricultural biodiversity: pest management and other benefits. Basic and Applied Ecology, Berlin, v.4, n.2, p.107-116, 2003. Available from: https://doi.org/10.1078/1439-1791-00122>. Accessed: Aug. 27, 2016. doi: 10.1078/1439-1791-00122.
https://doi.org/10.1078/1439-1791-00122...
; JACTEL et al., 2005JACTEL, H. et al. A test of the biodiversity-stability theory: meta-analysis of tree species diversity effects on insect pest infestations, and re-examination of responsible factors. In: SCHERER-LORENZEN, M.; KÖRNER, C.; SCHULZE, E.D. Forest Diversity and Function. Berlin: Springer, 2005. Chap.12. p.235-262.; LIN, 2011LIN, B.B. Resilience in agriculture through crop diversification: adaptive management for environmental change. BioScience, Oxford, v.61, n.3, p.183-193, 2011. Available from: https://doi.org/10.1525/bio.2011.61.3.4>. Accessed: Sept. 24, 2016. doi: 10.1525/bio.2011.61.3.4.
https://doi.org/10.1525/bio.2011.61.3.4...
). Trees for shading and green manures (cover crops) have been used in coffee plantings (RESENDE et al., 2007RESENDE, A.L.S. et al. Ocorrência de parasitóides do bicho-mineiro infestando seis cultivares de café arábica em sistema orgânico com e sem arborização. Revista Brasileira de Agroecologia, Porto Alegre, v.2, n.2. p.921-924, 2007. Available from: http://aba-agroecologia.org.br/revistas/index.php/rbagroecologia/article/view/7115/5230>. Accessed: Aug. 27, 2016.
http://aba-agroecologia.org.br/revistas/...
; AMARAL et al., 2010AMARAL, D.S. et al. Does vegetational diversification reduce coffee leaf miner Leucoptera coffeella (Guérin-Mèneville) (Lepidoptera: Lyonetiidae) attack?. Neotropical Entomology, Londrina, v.39, n.4, p.543-548, 2010. Available from: http://dx.doi.org/10.1590/S1519-566X2010000400012>. Accessed: Aug. 27, 2016. doi: 10.1590/S1519-566X2010000400012.
http://dx.doi.org/10.1590/S1519-566X2010...
; LOMELÍ-FLORES et al., 2010LOMELÍ-FLORES, J.R. et al. Impacts of weather, shade cover and elevation on coffee leafminer Leucoptera coffeella (Lepidoptera: Lyonetiidae) population dynamics and natural enemies. Crop Protection, Amsterdam, v.29, n.9, p.1039-1048, 2010. Available from: https://doi.org/10.1016/j.cropro.2010.03.007>. Accessed: Aug. 27, 2016. doi: 10.1016/j.cropro.2010.03.007.
https://doi.org/10.1016/j.cropro.2010.03...
; SOUZA et al., 2014SOUZA, M.M. Nesting of social wasps (Hymenoptera: Vespidae) in a riparian forest of rio das Mortes in southeastern Brazil. Acta Scientiarum: Biological Sciences, Maringá, v.36, n.2, p.189-196, 2014. Available from: http://dx.doi.org/10.4025/actascibiolsci.v36i2.21460>. Accessed: Aug. 29, 2017. doi: 10.4025/actascibiolsci.v36i2.21460.
http://dx.doi.org/10.4025/actascibiolsci...
; THEODORO et al., 2014THEODORO, V.C.A. et al. Infestation by Leucoptera coffeella and leaf levels of total soluble sugar and protein in organic coffees. Coffee Science, Lavras, v.9, n.3, p.300-311, 2014. Available from: http://www.coffeescience.ufla.br/index.php/Coffeescience/article/view/638/pdf_96>. Accessed: Aug. 27, 2016.
http://www.coffeescience.ufla.br/index.p...
). Proper usage and management of these plants could improve the sustainability and quality of coffee yields.

Studies have shown that coffee agroecosystem diversification increases the occurrence of CLM’s natural enemies (DE LA MORA et al., 2008DE LA MORA, A. Arboreal ant abundance and leaf miner damage in coffee agroecosystems in Mexico. Biotropica, Hoboken, v.40, n.6, p.742-746, 2008. Available from: http://onlinelibrary.wiley.com/doi/10.1111/j.1744-7429.2008.00444.x/full>. Accessed: Aug. 29, 2017. doi: 10.1111/j.1744-7429.2008.00444.x.
http://onlinelibrary.wiley.com/doi/10.11...
; REZENDE et al., 2014REZENDE, M.Q. et al. Extrafloral nectaries of associated trees can enhance natural pest control. Agriculture, Ecosystems & Environment, Amsterdam, v.188, p.198-203, 2014. Available from: https://doi.org/10.1016/j.agee.2014.02.024>. Accessed: Aug. 27, 2016. doi: 10.1016/j.agee.2014.02.024.
https://doi.org/10.1016/j.agee.2014.02.0...
; PACK et al., 2015PAK, D. et al. Parasitoid wasps benefit from shade tree size and landscape complexity in Mexican coffee agroecosystems. Agriculture, Ecosystems & Environment, Amsterdam, v.206, p.21-32, 2015. Available from: https://doi.org/10.1016/j.agee.2015.03.017>. Accessed: Aug. 29, 2017. doi: 10.1016/j.agee.2015.03.017.
https://doi.org/10.1016/j.agee.2015.03.0...
). However, a simple increase in agroecosystem diversity may not ensure an increase in biological control (TSCHARNTKE et al., 2016TSCHARNTKE, T. et al. When natural habitat fails to enhance biological pest control - Five hypotheses. Biological Conservation, Amesterdã, v.204, n.2, p.449-458, 2016. Available from: https://doi.org/10.1016/j.biocon.2016.10.001>. Accessed: Aug. 29, 2017. doi: 10.1016/j.biocon.2016.10.001.
https://doi.org/10.1016/j.biocon.2016.10...
). AMARAL et al., 2010AMARAL, D.S. et al. Does vegetational diversification reduce coffee leaf miner Leucoptera coffeella (Guérin-Mèneville) (Lepidoptera: Lyonetiidae) attack?. Neotropical Entomology, Londrina, v.39, n.4, p.543-548, 2010. Available from: http://dx.doi.org/10.1590/S1519-566X2010000400012>. Accessed: Aug. 27, 2016. doi: 10.1590/S1519-566X2010000400012.
http://dx.doi.org/10.1590/S1519-566X2010...
reported that coffee intercropped with banana trees (Musa spp.) was not able to reduce CLM occurrence. Thus, effects of different coffee intercropping systems on CLM and wasp occurrence are still largely unknown.

Leucaena plants (Leucaena leucocephala L.) have been used to protect crop plants against frost (VALENTINI et al., 2010VALENTINI, L.S.P. et al. Air temperature in unshaded arabic coffee systems and arborized with rubber tree and dwarf coconut palm at Mococa region, state of São Paulo, Brazil. Bragantia, Campinas, v.69, n.4, p.1005-1010, 2010. Available from: http://dx.doi.org/10.1590/S0006-87052010000400028>. Accessed: Aug. 27, 2016. doi: 10.1590/S0006-87052010000400028.
http://dx.doi.org/10.1590/S0006-87052010...
) and to enrich soil organic matter (GUIMARÃES et al., 2014GUIMARÃES, G.P. et al. Soil aggregation and organic carbon of Oxisols under coffee in agroforestry systems. Revista Brasileira de Ciências do Solo, Viçosa, v.38, n.1, p.278-287, 2014. Available from: http://dx.doi.org/10.1590/S0100-06832014000100028>. Accessed: Aug. 27, 2016. doi: 10.1590/S0100-06832014000100028.
http://dx.doi.org/10.1590/S0100-06832014...
). Pigeon pea plants [Cajanus cajan (L. Millsp.)], in addition to being used for the protection of young plants against frost (CARAMORI et al., 1999CARAMORI, P.H. et al. Temporary shading of young coffee plantations with pigeon pea (Cajanus cajan) for frost protection in Southern Brazil. Revista Brasileira de Agrometeorologia, Sete Lagoas, v.7, n.2, p.195-200, 1999.), have also been used to improve soil quality and may be used to feed people and livestock (AZEVEDO et al., 2007AZEVEDO, R.L. et al. Feijão guandu, uma planta multiuso. Revista da Fapese, Aracaju, v.3, n.2, p.81-86, 2007. Available from: http://www.fapese.org.br/revista_fapese/v3n2/artigo8.pdf>. Accessed: Aug. 27, 2016.
http://www.fapese.org.br/revista_fapese/...
). However, there is a lack of knowledge of how leucaena and pigeon pea plants affect CLM occurrence. Coffee plantings intercropped with these plants could affect microclimate conditions (mostly temperature, humidity and ventilation) and, consequently, CLM infestation and predation by wasps.

Therefore, prevalence of CLM infestation (percentage of leaves with mines and mines per leaf) and of predation by wasps over a year and a half were compared in two organic farming systems: one shaded with leucaena and the other intercropped with pigeon pea.

MATERIALS AND METHODS:

Field surveys were conducted from June 2011 to December 2012 in two coffee plantings in Alvorada do Sul County, Brazil (22º 54’ 50” S, 51º 13’ 56” W; 532 m.a.s.l. and 22º 54’ 38” S, 51º 13’ 59” W; 530 m.a.s.l.). The two plantings were located only 400m apart. The regional climate is classified as humid subtropical with hot summers (Cfa). The mean temperature was 21.5ºC, and accumulated rainfall was 2318 mm during the study period (data from IAPAR meteorological station; see figure 1).

Figure 1
Monthly average values of temperature minimum (dotted line), average (filled line) and maximum (dashed line) and accumulated rainfall (columns) during the assessment period, June 2011 to December 2012, in Alvorada do Sul County, Paraná State, Brazil.

The two organic plantings utilized different coffee cultivation systems. In the first system, coffee plants cv. IAPAR 59 with four years of age were spaced 2m (lines) X 1m (plants within the lines) and were intercropped (shaded) with L. leucocephala trees of the same age planted with 2.5m X 5m spacing. In the second system, coffee plants (same cv. and spacing) were intercropped with pigeon pea plants (Cajanus cajan L.) (cultivar PPI 832), which were placed between coffee lines 0.5m apart. Fertilization varied according to cultivation systems. Shaded coffee received compost from poultry litter. Pigeon pea-intercropped coffee received compost from cattle manure plus crop residues. Compost (2kg/plant) was applied in both systems during the flowering period. Standard phytosanitary measures were not achieved during the study period.

Assessments of CLM infestation and wasp predation were conducted by establishing five sample points in each planting, each at least 10m apart. Each point included 10 coffee plants and sampled four random leaves per plant (N=40). The third pair of leaves (from the apex of the reproductive branch) was collected from the middle third of the plants (VILLACORTA & WILSON, 1994VILLACORTA, A.; WILSON, L.T. Plano de amostragem sequencial de presença-ausência do dano causado pelo bicho mineiro Leucoptera coffeella Guérin ­ Méneville. Anais da Sociedade Entomológica do Brasil, v.23, n.2, p.277­-284, 1994.); if the third pair was absent, the fourth pair was used.

Pest infestation was assessed by counting the number of leaves containing injuries (mines) and without predation traces (intact mines). The number of mines exhibiting signs of predation (mines lacerated by wasp mandibles) was also counted. Assessments were conducted from 09:00 to 12:00 every 15 days, for a total of 33 assessments.

Tests for normality and homogeneity of variance were performed to verify the assumptions for analysis of variance. Thereafter, groups were compared using a t test (P<0.01). The BioEstat 5.0 (Ayres 2007) software package was used.

RESULTS AND DISCUSSION:

We could not verify a relationship between CLM infestation and weather conditions recorded by the IAPAR meteorological station nearest the study areas. Although, weather conditions (at the regional level) were the same for the two areas, the occurrence of CLM was markedly different (Figure 1 and 2), probably due to the microclimatic effects that the intercropped plants (MORAIS et al., 2006MORAIS, H. et al. Microclimatic characterization and productivity of coffee plants grown under shade of pigeon pea in Southern Brazil. Pesquisa Agropecuária Brasileira, Brasília, v.41, n.5, p.763-770, 2006. Available from: http://dx.doi.org/10.1590/S0100-204X2006000500007>. Accessed: Aug. 27, 2016. doi: 10.1590/S0100-204X2006000500007.
http://dx.doi.org/10.1590/S0100-204X2006...
) or shaded trees (ARAÚJO et al., 2016ARAÚJO, A.V. Microclimate, development and productivity of robusta coffee shaded by rubber trees and at full sun. Revista Ciência Agronômica, Fortaleza, v.47, n.4, p.700-709, 2016. Available from: http://dx.doi.org/10.5935/1806-6690.20160084>. Accessed: Aug. 29, 2017. doi: 10.5935/1806-6690.20160084.
http://dx.doi.org/10.5935/1806-6690.2016...
) caused in each coffee planting.

Figure 2
Mean infestation prevalence (%) of the coffee leaf miner (CLM) in leucaena-shaded organic coffee (filled line) and pigeon pea-intercropped organic coffee plantings (dashed line) from June 2011 to December 2012, Paraná State, Brazil. The dotted line indicates the action level (AL) suggested by Reis & Souza, 1996REIS, P.R.; SOUZA, J.C. Manejo integrado do bicho-mineiro, Perileucoptera coffeella (Guérin-Mèneville) (Lepidoptera: Lyonetiidae), e seu reflexo na produção de café. Anais da Sociedade Entomológica do Brasil, v.25, n.1, p.77-82, 1996..

Pigeon pea-intercropped coffee presented fewer CLM infestations and number of mines per leaf than the leucaena-shaded coffee (Figure 3A and 3B). Evidence of predation of the CLM by wasps was more common in leucaena-shaded coffee than pigeon pea-intercropped coffee (Figure 3C).

Figure 3
Mean (± SD) infestation prevalence of the coffee leaf miner (CLM) (A); number of mines per leaf (B) and prevalence of mines with signs of predation by wasps (lacerated mines) (C) in leucaena-shaded organic coffee and pigeon pea-intercropped organic coffee plantings from June 2011 to December 2012, in Alvorada do Sul County, Paraná State, Brazil.

CLM infestation in pigeon pea-intercropped coffee was above the action level (AL) of 30% (see REIS & SOUZA, 1996REIS, P.R.; SOUZA, J.C. Manejo integrado do bicho-mineiro, Perileucoptera coffeella (Guérin-Mèneville) (Lepidoptera: Lyonetiidae), e seu reflexo na produção de café. Anais da Sociedade Entomológica do Brasil, v.25, n.1, p.77-82, 1996.) at the beginning of the assessments; however, during all of 2012, infestation was below the AL (Figure. 3). In leucaena-shaded coffee, infestation was below AL only during November 2011 and remained above it for all other assessments. This is typical of the pest in the conventional plantings close to the experimental areas, in which farmers must spray several times during the production cycle.

Our observation of lower infestation of CLM in pigeon pea-intercropped plantings corroborates a previous study performed by THEODORO et al., 2014THEODORO, V.C.A. et al. Infestation by Leucoptera coffeella and leaf levels of total soluble sugar and protein in organic coffees. Coffee Science, Lavras, v.9, n.3, p.300-311, 2014. Available from: http://www.coffeescience.ufla.br/index.php/Coffeescience/article/view/638/pdf_96>. Accessed: Aug. 27, 2016.
http://www.coffeescience.ufla.br/index.p...
. In general, when coffee seedlings are planted between pigeon pea lines (“tunnels”), fewer CLM are observed (CARAMORI, 2000CARAMORI, P. H. et al. Métodos de proteção contra geadas em cafezais em formação. 2000. Available from: http://www.iapar.br/arquivos/File/zip_pdf/protgeada.pdf>. Accessed: Aug. 27, 2016.
http://www.iapar.br/arquivos/File/zip_pd...
). Microclimate is affected when pigeon pea is intercropped between coffee seedlings, and adult planting protects the plants from frost and wind (MORAIS et al., 2006MORAIS, H. et al. Microclimatic characterization and productivity of coffee plants grown under shade of pigeon pea in Southern Brazil. Pesquisa Agropecuária Brasileira, Brasília, v.41, n.5, p.763-770, 2006. Available from: http://dx.doi.org/10.1590/S0100-204X2006000500007>. Accessed: Aug. 27, 2016. doi: 10.1590/S0100-204X2006000500007.
http://dx.doi.org/10.1590/S0100-204X2006...
; CARAMORI et al., 1999). As a result, CLM population dynamics may also be affected. The lower daytime temperature in coffee intercropped with pigeon pea (MORAIS et al., 2006) may negatively influence CLM development (LOMELÍ-FLORES et al., 2010LOMELÍ-FLORES, J.R. et al. Impacts of weather, shade cover and elevation on coffee leafminer Leucoptera coffeella (Lepidoptera: Lyonetiidae) population dynamics and natural enemies. Crop Protection, Amsterdam, v.29, n.9, p.1039-1048, 2010. Available from: https://doi.org/10.1016/j.cropro.2010.03.007>. Accessed: Aug. 27, 2016. doi: 10.1016/j.cropro.2010.03.007.
https://doi.org/10.1016/j.cropro.2010.03...
). Intercropping pigeon pea plants in coffee planting also alters nutrient dynamics in the soil and affects CLM indirectly. Total soluble sugars are also affected by organic fertilizers and thus may also affect CLM (THEODORO et al., 2014).

CLM infestations during the coldest months were previously reported under shaded conditions (LOMELÍ-FLORES et al., 2010LOMELÍ-FLORES, J.R. et al. Impacts of weather, shade cover and elevation on coffee leafminer Leucoptera coffeella (Lepidoptera: Lyonetiidae) population dynamics and natural enemies. Crop Protection, Amsterdam, v.29, n.9, p.1039-1048, 2010. Available from: https://doi.org/10.1016/j.cropro.2010.03.007>. Accessed: Aug. 27, 2016. doi: 10.1016/j.cropro.2010.03.007.
https://doi.org/10.1016/j.cropro.2010.03...
), but this was not the case in our present study (Figure 3). A combination of factors may be associated with the differences in CLM populations among the farming systems. Although, poultry litter has been previously reported to reduce CLM damage (THEODORO et al., 2014THEODORO, V.C.A. et al. Infestation by Leucoptera coffeella and leaf levels of total soluble sugar and protein in organic coffees. Coffee Science, Lavras, v.9, n.3, p.300-311, 2014. Available from: http://www.coffeescience.ufla.br/index.php/Coffeescience/article/view/638/pdf_96>. Accessed: Aug. 27, 2016.
http://www.coffeescience.ufla.br/index.p...
), infestations in the leucaena-shaded coffee treatment (which was fertilized with poultry litter) were higher than in the treatment with pigeon pea intercropping (Figure 2A and B). In addition to leaf nutritional condition, the headspace volatiles in the planting may affect CLM dynamics because coffee volatiles can influence CLM mating behavior (FONSECA et al., 2013FONSECA, M.G. et al. Influence of host plant on reproductive behavior of Leucoptera coffeella (Guérin-Mèneville) (Lepidoptera: Lyonetiidae). Coffee Science, Lavras, v.8, n.1, p.101-108, 2013. Available from: http://www.sbicafe.ufv.br:80/handle/123456789/7937>. Accessed: Aug. 27, 2016.
http://www.sbicafe.ufv.br:80/handle/1234...
). Pigeon pea probably affected CLM behavior as well; this plant has been reported to have insect-repellent proprieties (ROMEIS et al., 1998ROMEIS, J. et al. Physical and chemical plant characters inhibiting the searching behaviour of Trichogramma chilonis. Entomologia Experimentalis et Applicata, v.87, n.3, p.275-284, 1998. Available from: http://onlinelibrary.wiley.com/doi/10.1046/j.1570-7458.1998.00332.x/epdf>. Accessed: Aug. 27, 2016. doi: 10.1046/j.1570-7458.1998.00332.x.
http://onlinelibrary.wiley.com/doi/10.10...
, OBICO & RAGRARIO, 2014OBICO, J.J.A.; RAGRARIO, E.M. A survey of plants used as repellents against hematophagous insects by the Ayta people of Porac, Pampanga Province, Phillippines. Philippine Science Letter, v.7, n.1, p.189-196, 2014. Available from: http://philsciletters.org/2014/PSL%202014-vol07-no01-p179-186%20Obico.pdf>. Accessed: Aug. 27, 2016.
http://philsciletters.org/2014/PSL%20201...
). Additional studies must be conducted to confirm CLM repellence by pigeon pea plants compared with coffee plants.

Predatory wasps are the principal natural enemies of CLM and regulate pest populations under field conditions (TUELHER et al., 2003TUELHER, E.S. et al. Occurrence of coffee leaf-miner (Leucoptera coffeella) influenced by season and altitude. Acta Scientiarum: Agronomy, Maringá, v.25, n.1, p.119-124, 2003. Available from: http://dx.doi.org/10.4025/actasciagron.v25i1.2458>. Accessed: Aug. 29, 2017. doi: 10.4025/actasciagron.v25i1.2458.
http://dx.doi.org/10.4025/actasciagron.v...
; PEREIRA et al., 2007PEREIRA, E.J.G. et al. Seasonal mortality factors of the coffee leaf miner, Leucoptera coffeella. Bulletin of Entomological Research, Cambridge, v.97, n.4, p.421-432, 2007. Available from: https://doi.org/10.1017/S0007485307005202>. Accessed: Aug. 27, 2016. doi: 10.1017/S0007485307005202.
https://doi.org/10.1017/S000748530700520...
; SCALÓN et al., 2011SCALÓN, J.D. et al. Spatial and temporal dynamics of coffee-leaf-miner and predatory wasps in organic coffee field in formation. Ciência Rural, Santa Maria, v.41, n.4, p.646-652, 2011. Available from: http://dx.doi.org/10.1590/S0103-84782011005000037>. Accessed: Aug. 27, 2016. doi: 10.1590/S0103-84782011005000037.
http://dx.doi.org/10.1590/S0103-84782011...
). High abundances of natural enemies in organic farming systems have also been previously reported (ALTIERI & NICHOLLS, 2004ALTIERI, M.A.; NICHOLLS, C.I. Biodiversity and pest management in agroecosystems. Haworth Press, New York, 240p, 2004.), probably due to lower anthropogenic disturbance and higher plant diversity (BIANCHI et al. 2006BIANCHI, F.J.J.A. et al. Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Proceedings of the Royal Society B: Biological Sciences, London, v.273, n.1595, p.1715-1727, 2006. Available from: https://doi.org/10.1098/rspb.2006.3530>. Accessed: Aug. 27, 2016. doi: 10.1098/rspb.2006.3530.
https://doi.org/10.1098/rspb.2006.3530...
).

Higher predation of CLM mines in the leucaena-shaded coffee than pigeon pea-intercropped coffee (Figure 2C) may be associated with a density-dependent relationship due to differences in the availability of the prey (Figures. 2 and 3). The density-dependent relationship between predatory wasps and CLM has been previously described (FERNANDES et al. 2009FERNANDES, F.L. et al. Effects of irrigation, environmental variability and predatory wasp on Leucoptera coffeella (Guérin-Méneville) (Lepidoptera: Lyonetiidae), in coffee plants. Neotropical Entomology , Londrina, v.38, n.3, p.410-417, 2009. Available from: http://dx.doi.org/10.1590/S1519-566X2009000300018>. Accessed: Aug. 29, 2017. doi: 10.1590/S1519-566X2009000300018.
http://dx.doi.org/10.1590/S1519-566X2009...
). This hypothesis is supported by the fact that predatory wasps are attracted to volatiles emitted by coffee plants damaged by CLM (FERNANDES et al., 2010FERNANDES, F.L. et al. Coffee volatiles and predatory wasps (Hymenoptera: Vespidae) of the coffee leaf miner Leucoptera coffeella. Sociobiology, Feira de Santana, v.56, n.2, p.455-464, 2010. Available from: https://www.researchgate.net/publication/282135859_Coffee_Volatiles_and_Predatory_Wasps_Hymenoptera_Vespidae_of_the_Coffee_Leaf_Miner_Leucoptera_coffeella>. Accessed: Aug. 27, 2016.
https://www.researchgate.net/publication...
). Leucaena plants also have extrafloral nectaries (FREITAS et al., 2001FREITAS, L.H.C. et al. Intra and intergenotype variability in a population of hybrids between Leucaena leucocephala and L. diversifolia. Pesquisa Agropecuária Brasileira, Brasília, v.36, n.8, p.1069-1076, 2001. Available from: http://dx.doi.org/10.1590/S0100-204X2001000800009>. Accessed: Aug. 27, 2016. doi: 10.1590/S0100-204X2001000800009.
http://dx.doi.org/10.1590/S0100-204X2001...
), which may also attract wasps to the coffee planting. Furthermore, leucaena plants may serve as a suitable shelter for establishing wasp nests, since the wasps prefer tree like plants rather than shrubs or herbaceous plants (SOUZA et al., 2014SOUZA, T.P. et al. Seasonal occurrence, predation and parasitism of Leucoptera coffeella (Guérin-Méneville, 1842) (Lepidoptera: Lyonetiidae) in coffee Plants cssociated with grevilla trees. Coffee Science, Lavras, v.9, n.1, p.34-50, 2014. Available from: http://www.coffeescience.ufla.br/index.php/Coffeescience/article/view/531/pdf_52>. Accessed: Aug. 27, 2016.
http://www.coffeescience.ufla.br/index.p...
).

The information obtained in our study may be used to design more resilient coffee-producing agroecosystems. One option to maximize the beneficial effects of both leucaena and pigeon pea plants in coffee plantings to reduce CLM would be the inclusion of both plant species, for example, intercropping pigeon pea and using leucaena as a windbreak. If beneficial additive effects of these species on CLM infestations could be achieved, it seems likely that the action level would not be reached. However, for wide spread utilization by farmers to be effective, additional studies must be conducted to determine optimal management of these plants (densities, spacing, cultivars, pruning, etc.) and their multifunctional effects (yields, weed suppression, frost protection, reduced erosion, soil fertility improvement, etc.) and constraints on their use in coffee plantings (labor, interference with cultivation practices, excessive shading, etc.).

CONCLUSION :

We observed fewer CLM mines on leaves of coffee plants in the pigeon pea-intercropped planting than in the leucaena-shaded planting. More signs of CLM predation by wasps were observed in the leucaena-shaded than the pigeon pea-intercropped planting

ACKNOWLEDGEMENTS:

To the farmers that allowed the study in their areas. To Brazilian consortium of coffee research and development, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) by grants for the authors.

REFERENCES:

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    CR-2016-0863.R2

Publication Dates

  • Publication in this collection
    2018

History

  • Received
    19 Sept 2016
  • Accepted
    11 Jan 2018
  • Reviewed
    10 Apr 2018
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