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

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Title:
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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English
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Stuart, Tyler H
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Atta (Insects)--Costa Rica   ( lcsh )
Coffee--Costa Rica--Puntarenas--Canitas   ( lcsh )
Agricultural ecology--Costa Rica   ( lcsh )
Atta(Insectos)--Costa Rica
Café--Costa Rica--Puntarenas--Cañitas
Ecología agrícola--Costa Rica
Tropical Ecology 2008
Coffee cultivation, effect on leaf-cutter ants
Ecología Tropical 2008
Cultivo de café, efecto en las hormigas sompopas
Genre:
Reports   ( lcsh )
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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Text in English.
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Born Digital

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1nnr nnr nnr nnr r r r r nnrn nnrn nnrn nnrnr r r r nnnr nnnr nnnr nnnr !"nn !"nn !"nn !"nn #nn$%&rrn% ABSTRACT The addition of a specific group of rapid-growth sh ade tree species to coffee in monoculture, or the inclusion of these species in shade-grown coffee, m ay reduce leaf herbivory by Atta cephalotes This study was conducted in Caitas, 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-coff ee, 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 mor e 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. RESUMEN La adicin de un grupo especfico de especies de r boles que dan sombra y crecen rpido al caf en monocultivo, o la inclusin de estas especies en c af que crece en la sombra, podra reducir la herbi vora de las hojas por Atta cephalotes Este estudio fue conducido en Caitas, Costa Ric a en tres parcelas—crece en la sombra, monocultivo, y no caf—dentro de plan taciones de caf, cada una de las cuales tena una colonia diferente de A. cephalotes Despus de observar el mtodo de seleccin por l as hormigas entre cuatro especies de rboles que dan sombra que no te nan caf y dos variedades de caf, Caturra y Katwa y, los resultados indicaron que las hormigas no tenan preferencias por las especies probados dentro de c ada parcela (Sombra: K-W = 0.976, p = 0.98; Monocultivo: K-W = 1.319, p = 0.971; No caf: K-W = 0.803, p = 0.992; Todos: df = 6, n = 35). Las hormigas esco gieron ms frecuentemente Erythrina lanceolata en la parcela de caf que crece en la sombra que las otra s (K-W = 7.22, n = 15, df = 2, p = 0.027). Estos resultados podran tener implicaciones importantes para ambos la labranza de caf y la restauracin 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 larg er trees that provide the soil with

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2 nutrients, and also in monoculture. The latter met hod removes all trees and replaces old varieties of coffee with new sun-loving varieties ( Perfecto and Snelling 1995). The majority of coffee in Central America is grown in m onoculture (Perfecto and Snelling 1995), which reduces biodiversity and increases cro p vulnerability to pests. Expensive fossil 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 noncoffee, shade tree species 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 fo und in all types of forest (Stevens 1983); they especially like gap areas (Blanton and Ewel 1985). Though originally considered a generalist forager, studies support th at A. cephalotes attacks plants selectively (Rockwood 1976, Howard 1988). Among th e selections of A. cephalotes are several Neotropical crops grown in monoculture (Bla nton 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 origin al biodiversity of these disturbed areas is extremely important. Changes in biodiversity in agricultural areas and other areas of high human impact have not been stud ied as extensively as those in more natural habitats. A study of coffee farming in Mex ico found traditional coffee growing methods to only partially disturb original forests (Moguel and Toledo 1999). Therefore, these traditional, shade-grown coffee plantations c an have high species richness and may be important homes for many organisms, including pl ants and arthropods. It is, therefore, highly beneficial for both the farmers and the envi ronment 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 potential ly be grown with coffee. A recent study at a farm in San Luis, Costa Rica, s tudied leaf preferences of A. cephalotes with several shade tree species and coffee varieti es (Hannemann 2007). Results from this study suggeste d a preference for the tree species over the coffee. This study only focused on two si tes, in one farm: in monoculture coffee and in secondary forest. Based on this previous st udy it is expected that A. cephalotes will show a preference towards non-coffee shade tre es, therefore showing that shade trees may offer practical uses for farmers in reducing le af herbivory of coffee. It may also provide an opportunity to restore some biodiversity to habitats struggling 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 f arms in Caitas, Costa Rica, from April 15 to May 3, 2008. Each plot investigated a separate ant colony. The ShadeGrown Plot had both varieties of shade-grown C. arabica Caturra and Katway, within close proximity to the ant nest. The Monoculture P lot was approximately three meters

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3 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. The following shade tree species (Table 1) were sel ected 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. arabica and also for a control extract, which did not hav e any plant material. ___________________________________________________ _____________________ TABLE 1. Family, Genus and species of the six pla nts 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 medium for extracts whe n testing plant preference in leafcutter 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 ra tio. Each solution was ground for ten minutes. Each solution was then strained into separate film canisters and each shaken to complete mixing. The control extract was methan ol and hydrochloric acid with no leaf matter. Approximately 50 oats were placed in the s trainer for each extract application and an eyedropper was used to apply the plant extra cts 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 oa ts 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 line across the ant trail. The quantities removed from the stock of each extract were observe d and recorded for two hours or until the supply of one extract ran out. Each time an an t removed an oat from the starting position and carried it toward the colony, 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 frequ ently depleted the daily supply of one or more extract, daily removal quantities were modi fied 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 preferen ces of each extract in and among each plot. RESULTS A. cephalotes exhibited equal selection of all of the plant extra cts within the Shade-Grown Plot (Table 2). The same was true with in the Monoculture Plot and the No-Coffee Plot (Table 2). ___________________________________________________ _____________________ TABLE 2. Kruskal-Wallis values show no difference f or A. cephalotes preference of three plots on coffee farms, evaluated for six plan t extracts ( E. lanceolata S. glandulosum C. costaricensis A. arborescens C. arabica [Caturra], and C. arabica [Katway]) and a control extract, in Caitas, 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-Walli s = 7.22, df = 2, p = 0.027, n = 15; Fig. 1, Table 3), followed by the No-Coffee Plot (averag e 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-grownMonocultureNo-Coffee PlotAverage 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 Caitas, 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. arborescens 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 Caitas, Costa Rica. Shade-Grown Plot grows shade coffee ( C. arabica ) of Caturra and Katway varieties; Monoculture Plot grows both varieties in monocultur e; No-Coffee Plot is a field of tall grass with no coffee. Each of the th ree 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 0.613 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 beneficia l for reducing herbivory on coffee leaves in Caitas, Costa Rica. A. cephalotes 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 targets for the ants, allevi ating 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 concentrations of tannins, carbon -based metabolites in leaves that are used for defense against herbivory, are known to va ry based on available nutrients and light (Denslow et al. 1987, Mole et al. 1988) durin g leaf maturation. Therefore, there

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6 may be certain ages or growth conditions at which a nts 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 coffee. This may offer particular benefits to farmers who already pr actice 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 already frequently plant and prune nitrogen-fixing legumes as a method of soil n itrification (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 befo re for nitrification on coffee farms. E. lanceolata S. glandulosum C. costaricensis and A. arborescens are all known as fast-growing species, which need little maintena nce, and grow well in disturbed areas. Many of these species also can propagate from cutti ngs (Stevens 1983), which minimizes time to maturity. Therefore, the easy fast establi shment 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 10 0% germination rates when sown (Woolliams 1979). Cutt ings from A. arborescens can be grown as living fence posts, serving multiple purpo ses as coffee shade, fence post, and a target for A. cephalotes (Haber et al. 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 pollination, by either passerine birds or hummingbirds (Neill 1988). Wasp s visit S. glandulosum while small moths and stingless bees pollinate C. costaricensis (Haber et al. 2000). A. arborescens attracts bees, beetles, butterflies, and occasional ly hummingbirds for pollination (Haber et al. 2000). The addition of even these few speci es of shade trees to a monoculture or shade-grown coffee plantation has great potential t o allow the establishment of numerous animal populations to an area with low biodiversity A. cephalotes is also known to cut non-leaf plant parts, includin g flower buds. During this study, I observed ants at all of the pl ots carrying large quantities of multiple, unidentified flower buds to the nests. A further s tudy 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 c offee for both farmers and biodiversity. Leaf toughness is the most effective defense against herbivory (Coley and Barone 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, multi ple farmers and residents of the plots stressed the high amounts of damage that A. cephalotes does to both roses and Heliconia so either of these plants may offer additional stud ies in Caitas, Costa Rica. Finally, a study could look at leaf-cutter ant damage to coffe e plants in monocultures versus shadegrown coffee plants. ACKNOWLEDGEMENTS

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7I would like to thank Tania Chavarra for her sugge stions in refining my methods, and for her assistan ce with analyzing the results of the study. I would a lso like to thank Karen Masters for her assistance in selecting appropriate shade tree species, as well a s 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 Jimenz and Victor Torres Rojas for allowing me access to their coffee plantations. Finally, thanks to Josh Coope r 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 management 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 tropica l ecosystems. Ecology. 66(3): 861-869. Coley, P.D. and J.A. Barone. 1996. Herbivory and pl ant 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 ra in 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 I ntroduction to Cloud Forest Trees: Monteverde, Costa Rica (2nd Ed). Mountain Gem Publications. Monteverde, 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 physi cal 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 fo rest conversion. Ecol. Apps. 10(6): 16331647. Moguel, P. and V.M. Toledo. 1999. Biodiversity cons ervation in traditional coffee systems of Mexico. Cons. Bio. 13(1): 11-21. Mole, S., J.A.M. Ross, and P.G. Waterman. 1988. Lig ht-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 R elationships in Erythrina (Leguminosae: Papilionoideae). Annals of the Missouri Bot. Garden 75(3): 886-969. Perfecto, I. and R. Snelling. 1995. Biodiversity an d the transformation of a tropical agroecosystem: a nts in coffee plantations. Ecol. Apps. 5(4): 1084-1097. Rockwood, L.L. 1972. The effect of defoliation on s eed production of six Costa Rican tree species. Ecology. 54(6): 1363-1369. -------. 1976. Plant selection and foraging pattern s in two species of leaf-cutting ants ( Atta ). Ecology. 57(1): 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. Woolliams, K.R. 1979. Notes on propagation and cult ivation of Erythrina in Hawaii. Annals of the Missouri Bot. Garden. 66(3): 541-544.


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El uso de rboles de sombra para reducir la herbivora en hojas de Coffea arabica por Atta cephalotes (Formicidae) en las fincas de Caitas, 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 Caitas, Puntarenas, Costa Rica
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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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Atta (Insects)--Costa Rica
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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Tropical Ecology 2008
Coffee cultivation, effect on leaf-cutter ants
Ecologa Tropical 2008
Cultivo de caf, efecto en las hormigas sompopas
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Reports
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CIEE
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t Monteverde Institute : Tropical Ecology
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