Use of shade trees to reduce leaf herbivory of Coffea arabica by Atta cephalotes (Formicidae) on farms in Cañitas, Puntarenas, Costa Rica


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Use of shade trees to reduce leaf herbivory of Coffea arabica by Atta cephalotes (Formicidae) on farms in Cañitas, Puntarenas, Costa Rica

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Use of shade trees to reduce leaf herbivory of Coffea arabica by Atta cephalotes (Formicidae) on farms in Cañitas, Puntarenas, Costa Rica
Translated Title:
El uso de árboles de sombra para reducir la herbivoría en hojas de Coffea arabica por Atta cephalotes (Formicidae) en las fincas de Cañitas, Puntarenas, Costa Rica
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Stuart, Tyler H
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Text in English

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Atta (Insects) ( lcsh )
Atta (Insectos) ( lcsh )
Coffee ( lcsh )
Cafe ( lcsh )
Agricultural ecology ( lcsh )
Ecologia agricola ( lcsh )
Costa Rica--Guanacaste--Cañitas
CIEE Spring 2008
CIEE Primavera 2008
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Reports

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Abstract:
The addition of a specific group of rapid-growth shade tree species to coffee in monoculture, or the inclusion of these species in shade-grown coffee, may reduce leaf herbivory by Atta cephalotes. This study was conducted in Cañitas, Costa Rica on three plots—shade-grown, monoculture, and no coffee—within coffee plantations, each of which had a separate A. cephalotes colony. After observing the selection process of the leaf-cutter ants among four non-coffee, shade tree species and two varieties of coffee, Caturra and Katway, results indicated that the ants had no preference(s) of the tested species within any of the tested plots (Shade: K-W = 0.976, p = 0.98; Monoculture: K-W = 1.319, p = 0.971; No Coffee: K-W = 0.803, p = 0.992; All plots: df = 6, n = 35). The ants more frequently selected Erythrina lanceolata at the Shade-Grown Plot than the other two plots (K-W = 7.22, n = 15, df = 2, p = 0.027). These findings may have important implications for both coffee farming and the restoration of biodiversity in monoculture crops. ( ,,, )
Abstract:
La adición de un grupo específico de especies de árboles de rápido crecimiento que dan sombra al café en monocultivo, o la inclusión de estas especies en café que crece en la sombra, podría reducir la herbivoría de las hojas por Atta cephalotes. Este estudio se realizó en Cañitas, Costa Rica en tres parcelas (crecimiento en la sombra, el monocultivo, y donde no hay café) dentro de las plantaciones de café, cada uno de ellos tenía una colonia separada de A. cephalotes.
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Student affiliation : Department of Biology, Occidental College
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Monteverde Institute
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This item is licensed with the Creative Commons Attribution Non-Commercial No Derivative License. This license allows others to download this work and share them with others as long as they mention the author and link back to the author, but they can’t change them in any way or use them commercially.
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m39.459 ( USFLDC Handle )

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The addition of a specific group of rapid-growth shade tree species to coffee in monoculture, or the inclusion of these species in shade-grown coffee, may reduce leaf herbivory by Atta cephalotes. This study was conducted in Caitas, Costa Rica on three plotsshade-grown, monoculture, and no coffeewithin coffee plantations, each of which had a separate A. cephalotes colony. After observing the selection process of the leaf-cutter ants among four non-coffee, shade tree species and two varieties of coffee, Caturra and Katway, results indicated that the ants had no preference(s) of the tested species within any of the tested plots (Shade: K-W = 0.976, p = 0.98; Monoculture: K-W = 1.319, p = 0.971; No Coffee: K-W = 0.803, p = 0.992; All plots: df = 6, n = 35). The ants more frequently selected Erythrina lanceolata at the Shade-Grown Plot than the other two plots (K-W = 7.22, n = 15, df = 2, p = 0.027). These findings may have important implications for both coffee farming and the restoration of biodiversity in monoculture crops.
La adicin de un grupo especfico de especies de rboles de rpido crecimiento que dan sombra al caf en monocultivo, o la inclusin de estas especies en caf que crece en la sombra, podra reducir la herbivora de las hojas por Atta cephalotes. Este estudio se realiz en Caitas, Costa Rica en tres parcelas (crecimiento en la sombra, el monocultivo, y donde no hay caf) dentro de las plantaciones de caf, cada uno de ellos tena una colonia separada de A. cephalotes.
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Text in English.
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Coffee--Costa Rica--Puntarenas--Canitas
Agricultural ecology--Costa Rica
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Atta(Insectos)--Costa Rica
Caf--Costa Rica--Puntarenas--Caitas
Ecologa agrcola--Costa Rica
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1 Use of shade trees to reduce leaf herbivory of Coffea arabica by Atta cephalotes Formicidae on farms in Cañitas, Puntarenas, Costa Rica Tyler H. Stuart Department of Biology, Occidental College ABSTRACT The addition of a specific group of rapid grow th shade tree species to coffee in monoculture, or the inclusion of these species in shade grown coffee, may reduce leaf herbivory by Atta cephalotes . This study was conducted in Cañitas, Costa Rica on three plots € shade grown, monoculture, and no coffee € w ithin coffee plantations, each of which had a separate A. cephalotes colony. After observing the selection process of the leaf cutter ants among four non coffee, shade tree species and two varieties of coffee, Caturra and Katway, results indicated that th e ants had no preferences of the tested species within any of the tested plots Shade: K W = 0.976, p = 0.98; Monoculture: K W = 1.319, p = 0.971; No Coffee: K W = 0.803, p = 0.992; All plots: df = 6, n = 35. The ants more frequently selected Erythrina lanceolata at the Shade Grown Plot than the other two plots K W = 7.22, n = 15, df = 2, p = 0.027. These findings may have important implications for both coffee farming and the restoration of bi odiversity in monoculture crops . RESUMEN La adición de un grupo específico de especies de árboles que dan sombra y crecen rápido al café en monocultivo, o la inclusión de estas especies en café que crece en la sombra, podría reducir la herbivoría de las hojas por Atta cephalotes . Este estudio fue conducido e n Cañitas, Costa Rica en tres parcelas € crece en la sombra, monocultivo, y no café € dentro de plantaciones de café, cada una de las cuales tenía una colonia diferente de A. cephalotes . Después de observar el método de selección por las hormigas entre cuatro especies de árboles que dan sombra que no tenían café y dos variedades de café, Caturra y Katway, los resultados indicaron que las hormigas no tenían preferencias por las especies probados dentro de cada parcela Sombra: K W = 0.976, p = 0.98; Monocultivo : K W = 1.319, p = 0.971; No café: K W = 0.803, p = 0.992; Todos: df = 6, n = 35. Las hormigas escogieron más frecuentemente Erythrina lanceolata en la parcela de café que crece en la sombra que las otras K W = 7.22, n = 15, df = 2, p = 0.027. Estos r esultados podrían tener implicaciones importantes para ambos la labranza de café y la restauración de biodiversidad en las cosechas de monoculture. INTRODUCTION Coffee is one of the most important and widespread crops in Central America. In Costa Rica, annual exports of coffee exceed $197 million. Coffee is grown in two ways: shade grown‚ in the understory, surrounded by larger trees that provide the soil with nutrients, and also in monoculture. The latter method removes all trees and replaces old var ieties of coffee with new sun loving varieties Perfecto and Snelling 1995. The

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2 majority of coffee in Central America is grown in monoculture Perfecto and Snelling 1995, which reduces biodiversity and increases crop vulnerability to pests. Expensive f ossil fuels are used as fertilizers or pesticides, but are difficult to obtain in the tropics Ewel 1986 and are not environmentally friendly. For this reason, farmers that use shade grown methods benefit from the ability of some non coffee, shade tree s pecies to return nitrogen to the soil. Atta cephalotes , a leaf cutting ant, can be found in many areas in the neotropics. It generally lives below 2000 meters, and can be found in all types of forest Stevens 1983; they especially like gap areas Bl anton and Ewel 1985. Though originally considered a generalist forager, studies support that A. cephalotes attacks plants selectively Rockwood 1976, Howard 1988. Among the selections of A. cephalotes are several Neotropical crops grown in monoculture Blanton and Ewel 1985, including cassava and coffee. Herbivory by A. cephalotes greatly negatively affects net productivity Rockwood 1972, undoubtedly creating a great concern for farmers. In addition to crop success, maintaining the original biodive rsity of these disturbed areas is extremely important. Changes in biodiversity in agricultural areas and other areas of high human impact have not been studied as extensively as those in more natural habitats. A study of coffee farming in Mexico found tra ditional coffee growing methods to only partially disturb original forests Moguel and Toledo 1999. Therefore, these traditional, shade grown coffee plantations can have high species richness and may be important homes for many organisms, including plant s and arthropods. It is, therefore, highly beneficial for both the farmers and the environment to design agricultural growth to mimic natural surrounding growth of the area. The objective of this study is to examine whether A. cephalotes shows preferences among two varieties of C. arabica and several shade tree species that could potentially be grown with coffee. A recent study at a farm in San Luis, Costa Rica, studied leaf preferences of A. cephalotes with several shade tree species and coffee varieties Hannemann 2007. Results from this study suggested a preference for the tree species over the coffee. This study only focused on two sites, in one farm: in monoculture coffee and in secondary forest. Based on this previous study it is expected that A. cephalotes will show a preference towards non coffee shade trees, therefore showing that shade trees may offer practical uses for farmers in reducing leaf herbivory of coffee. It may also provide an opportunity to restore some biodiversity to habitats st ruggling from monoculture practices. I hypothesize that because coffee can support the growth of various basidiomycete fungi Avelino et al. 2007, the ants will preferentially select the coffee varieties over the shade tree species within each study site . METHODS This study was performed on three plots in coffee farms in Cañitas, Costa Rica, from April 15 to May 3, 2008. Each plot investigated a separate ant colony. The Shade Grown Plot had both varieties of shade grown C. arabica , Caturra and Katway , within close proximity to the ant nest. The Monoculture Plot was approximately three meters from both a plot of monoculture Katway coffee and a plot of monoculture Caturra, and the No Coffee Plot lacked coffee and was made up of tall grasses and shrubs.

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3 The following shade tree species Table 1 were selected for this experiment because of their rapid growth and because they are native to the Monteverde area. Extracts were made from all four shade tree species, from Caturra and Katway varieties of C. ar abica , and also for a control extract, which did not have any plant material. ________________________________________________________________________ TABLE 1. Family, Genus and species of the six plants tested. Species Family Erythrina lanceolata Papillionaceae Sapium glandulosum Euphorbiaceae Citharexylum costaricensis Verbenaceae Acnistus arborescens Solanaceae C. arabica Caturra Rubiaceae C. arabica Katway Rubiaceae Plant extract and oat preparation Oats are commonly used as a medi um for extracts when testing plant preference in leaf cutter ants. From each plant, five grams of leaves were removed and added to 50 ml of 0.8 M methanol and 1% hydrochloric acid in a 1:1 ratio. Each solution was ground for ten minutes. Each solution w as then strained into separate film canisters and each shaken to complete mixing. The control extract was methanol and hydrochloric acid with no leaf matter. Approximately 50 oats were placed in the strainer for each extract application and an eyedropper was used to apply the plant extracts to the oats. The oats were then removed from the strainer and placed on a paper to dry. This was repeated several times to prepare for each day of experimentation. The oats were dried for at least an hour before use . Extract Preference Tests The study took place approximately five meters from the nest at each of the three sites. At each plot, five oats from each of the six plant extracts and the control extract were placed separately on to a piece of paper in a li ne across the ant trail. The quantities removed from the stock of each extract were observed and recorded for two hours or until the supply of one extract ran out. Each time an ant removed an oat from the starting position and carried it toward the colon y, the oat was replaced with another oat of the same extract. The plant extracts and control were placed in different positions every day to reduce any bias toward certain positions. This study was conducted five days at each plot, beginning at 8:30 AM. Because the ants frequently depleted the daily supply of one or more extract, daily removal quantities were modified to represent the quantity of oats removed in 60 minutes at a study site.

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4 Statistical Tests I used Kruskal Wallis tests to compare the p references of each extract in and among each plot. RESULTS A. cephalotes exhibited equal selection of all of the plant extracts within the Shade Grown Plot Table 2. The same was true within the Monoculture Plot and the No Coffee Plot Table 2. ______ __________________________________________________________________ TABLE 2. Kruskal Wallis values show no difference for A. cephalotes preference of three plots on coffee farms, evaluated for six plant extracts E. lanceolata , S. glandulosum , C. costaricen sis , A. arborescens , C. arabica [Caturra], and C. arabica [Katway] and a control extract, in Cañitas, Costa Rica. df n Kruskal Wallis value p value Shade Grown Plot 6 35 0.976 0.98 Monoculture Plot 6 35 1.319 0.971 No Coffee Plot 6 35 0.803 0.992 The ants selected E. lanceolata in the Shade Grown Plot more frequently than in the other sites daily average = 67 oats; Kruskal Wallis = 7.22, df = 2, p = 0.027, n = 15; Fig. 1, Table 3, followed by the No Coffee Plot average daily removal = 48 oats, and the Monoculture Plot removed the fewest E. lanceolata oats daily average = 29. 0 10 20 30 40 50 60 70 80 90 100 Shade-grown Monoculture No-Coffee Plot Average Oats Removed

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5 FIGURE 1. Difference in average daily removal of oats with E. lanceolata extract by A. cephalotes at three different plots Kruskal Wallis = 7.22, df = 2, p = 0.027, n = 15 in Cañitas, Costa Rica. A. cephalotes showed a trend toward selecting S. glandulosum more frequently at the Shade Grown Plot than the other plots Table 3. The ants did not show a preference among the plots with their selections of A. a rborescens , C. costaricensis , Caturra, or Katway Table 3. ________________________________________________________________________ TABLE 3. Kruskal Wallis values for A. cephalotes selection of oats of six plant extracts E. lanceolata , S. glandulosum , C . costaricensis , A. arborescens , C. arabica [Caturra], and C. arabica [Katway] and a control extract among three plots on coffee farms in Cañitas, Costa Rica. Shade Grown Plot grows shade coffee C. arabica of Caturra and Katway varieties; Monoculture P lot grows both varieties in monoculture; No Coffee Plot is a field of tall grass with no coffee. Each of the three plots has a separate A. cephalotes colony. df n Kruskal Wallis value p value Control 2 15 1.86 0.395 Caturra C. arabica 2 15 0.98 0.61 3 Katway C. arabica 2 15 1.52 0.468 Erythrina lanceolata 2 15 7.22 0.027 Sapium glandulosum 2 15 5.58 0.061 Citharexylum costaricensis 2 15 2.56 0.278 Acnistus arborescens 2 15 1.22 0.543 DISCUSSION These results did not support the hypothesis that A. cephalotes would select more frequently for the coffee varieties than the shade tree species. Instead, these results suggest that designing shade grown may be beneficial for reducing herbivory on coffee leaves in Cañitas, Costa Rica. A. cephalote s did not display a preference for one or more of the shade tree species over the two varieties of C. arabica , but it did select all of the species equally at each plot. Therefore, planting these shade species among coffee plants would provide multiple ta rgets for the ants, alleviating the harvesting of coffee leaves. It has been shown that extracts from fast expanding young leaves in the Tropics are preferred for feeding and also support greater fungal growth Coley and Barone 1996. Also, the concentrat ions of tannins, carbon based metabolites in leaves that are used for defense against herbivory, are known to vary based on available nutrients and light Denslow et al. 1987, Mole et al. 1988 during leaf maturation. Therefore, there

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6 may be certain ages or growth conditions at which ants would selectively cut these shade species, in turn favoring coffee. Additionally, these results show that A. cephalotes more frequently select oats of the E. lanceolata extract at the Monoculture Plot in the shade grown c offee. This may offer particular benefits to farmers who already practice traditional coffee growing. E. lanceolata could be especially useful as a shade tree within an already shaded plot or plantation to reduce leaf herbivory. In addition, farmers alr eady frequently plant and prune nitrogen fixing legumes as a method of soil nitrification McGrath 2000, making E. lanceolata an even better option for a shade grown plantation. The ants may even be familiar with this species as it has been used before f or nitrification on coffee farms. E. lanceolata , S. glandulosum , C. costaricensis , and A. arborescens are all known as fast growing species, which need little maintenance, and grow well in disturbed areas. Many of these species also can propagate from cu ttings Stevens 1983, which minimizes time to maturity. Therefore, the easy fast establishment of these species Woolliams 1979 allows them to establish early in the typical, eight to ten year life of a coffee crop Stevens 1983. Fresh Erythrina seeds, up to three months old, often have up to 100% germination rates when sown Woolliams 1979. Cuttings from A. arborescens can be grown as living fence posts, serving multiple purposes as coffee shade, fence post, and a target for A. cephalotes Haber et a l. 2000. From an ecological standpoint, it is particularly exciting that equal selectivity of the tested plant species by A. cephalotes was observed. For example, all 112 species of Erythrina in the tropics and subtropics are adapted for bird pollinatio n, by either passerine birds or hummingbirds Neill 1988. Wasps visit S. glandulosum , while small moths and stingless bees pollinate C. costaricensis Haber et al. 2000. A. arborescens attracts bees, beetles, butterflies, and occasionally hummingbirds for pollination Haber et al. 2000. The addition of even these few species of shade trees to a monoculture or shade grown coffee plantation has great potential to allow the establishment of numerous animal populations to an area with low biodiversity. A. cephalotes is also known to cut non leaf plant parts, including flower buds. During this study, I observed ants at all of the plots carrying large quantities of multiple, unidentified flower buds to the nests. A further study could examine A. cephalotes selection among coffee flower buds and the buds of a collection of shade species to possibly strengthen the importance of shade grown coffee for both farmers and biodiversity. Leaf toughness is the most effective defense against herbivory Coley and Baro ne 1996. Using leaf fragments, as opposed to oats, in a similar study could provide valuable information about how planting shade tree species with varying leaf toughnesses would affect leaf herbivory of coffee. Also, multiple farmers and residents of t he plots stressed the high amounts of damage that A. cephalotes does to both roses and Heliconia , so either of these plants may offer additional studies in Cañitas, Costa Rica. Finally, a study could look at leaf cutter ant damage to coffee plants in mono cultures versus shade grown coffee plants.

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7 ACKNOWLEDGEMENTS I would like to thank Tania Chavarría for her suggestions in refining my methods, and for her assistance with analyzing the results of the study. I would also like to thank Karen Masters for h er assistance in selecting appropriate shade tree species, as well as helping to familiarize me with them. Also, thank you to Richard Fritzmeier for help with locating two of my research sites. Thanks to Juan Cruz Jim é nez and Victor Torres Rojas for allo wing me access to their coffee plantations. Finally, thanks to Josh Cooper for reviewing this paper. LITERATURE CITED Avelino, J., S. Cabut, B. Barboza, M. Barquero, R. Alfaro, C. Esquivel, J. Durand, and C. Cilas. 2007. Topography and crop managemen t are key factors for the development of American Leaf Spot epidemics on coffee in Costa Rica. Phytopathology. 97: 1532 1542. Blanton, C.M. and J.J. Ewel. 1985. Leaf cutting ant herbivory in successional and agricultural tropical ecosystems. Ecology. 663 : 861 869. Coley, P.D. and J.A. Barone. 1996. Herbivory and plant defenses in tropical forests. Ann. Review Ecol. and Systematics. 27: 305 335. Denslow, J.S., P.M. Vitousek and J.C. Schultz. 1987. Bioassays of nutrient limitation in a tropical rain forest soil. Oecologia Berlin. 74: 370 376. Ewel, J.J. 1986. Ann. Review Ecol. and Systematics. 17: 245 271. Haber, W.A., W. Zuchowski, and E. Bello. 2000. An Introduction to Cloud Forest Trees: Monteverde, Costa Rica 2 nd Ed. Mountain Gem Publications. Monte verde, CR, pp. 93, 123, 145. Hannemann, C. 2007. Use of shade trees among coffee crops as a control for herbivory by Atta cephalotes Formicidae. CIEE, Fall 2007. Howard, J.J. 1988. Leaf cutting ant diet selection: The relative influence of leaf chemistry and physical features. Ecology. 69: 250 260. McGrath, D.A., M.L. Duryea, N.B. Comerford, and W.P. Cropper. 2000. Nitrogen and phosphorus cycling in an Amazonian agroforest eight years following forest conversion. Ecol. Apps. 106: 1633 1647. Moguel, P. a nd V.M. Toledo. 1999. Biodiversity conservation in traditional coffee systems of Mexico. Cons. Bio. 131: 11 21. Mole, S., J.A.M. Ross, and P.G. Waterman. 1988. Light induced variation in phenolic levels in foliage of rain forest plants. Journ. Chem. Ecol . 14: 1 21. Neill, D.A. 1988. Experimental Studies on Species Relationships in Erythrina Leguminosae: Papilionoideae. Annals of the Missouri Bot. Garden. 753: 886 969. Perfecto, I. and R. Snelling. 1995. Biodiversity and the transformation of a tropi cal agroecosystem: ants in coffee plantations. Ecol. Apps. 54: 1084 1097. Rockwood, L.L. 1972. The effect of defoliation on seed production of six Costa Rican tree species. Ecology. 546: 1363 1369. ------. 1976. Plant selection and foraging patterns i n two species of leaf cutting ants Atta . Ecology. 571: 48 61. Stevens, G.C. 1983. Atta cephalotes Zompopas, Leaf cutting ants. pp. 688 691. In Costa Rican Natural History. D.H. Janzen Ed.. 1983. The University of Chicago Press, Chicago, IL. Woollia ms, K.R. 1979. Notes on propagation and cultivation of Erythrina in Hawaii. Annals of the Missouri Bot. Garden. 663: 541 544.


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