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Influencia de las condiciones del micro-hbitat en la abundancia de la enfermedad de ojo de gallo (Mycena citricolor) en Coffea arabica
Influence of microhabitat conditions on the abundance of American Leaf Spot Disease (Mycena citricolor) on Coffea arabica
Coffea arabica (Rubiaceae) is extremely important to the agriculture, economy, and culture of Costa Rica. The primary production of coffee centers on the use of shade-grown cultivation methods; even though this method yields high amounts of coffee, it also fosters conditions that are optimal for the growth of diseases, such as Mycena citricolor. This study aimed to determine which microhabitat conditions favor the growth of the disease. In
addition to proximity to forest, the orientation of fungi spots, placement of the disease on the branches, and presence of an agricultural crop near the plant was recorded. It was determined that there was a greater M. citricolor abundance on C. arabica when plants were located closer to the forest, closer to an agricultural crop, and when it resided on the middle branches of the plant. The study also concluded that the disease prefers westerly facing slopes. On a whole, topographical and environmental factors that produce low-light conditions have a significant effect on the development of M. citricolor; in understanding the impact of these characteristics, farmers are better informed on what microhabitats are most suitable for high coffee production and low disease transmission yields.
Coffea arabica (Rubiaceae) es sumamente importante para la agricultura, la economa y la cultura de Costa Rica. La produccin primaria del caf se centra en mtodos de cultivo bajo sombra; aunque este mtodo aumenta la produccin del caf, tambin fomenta condiciones que son ptimas para el crecimiento de las enfermedades como Mycena citricolor. El objetivo de este estudio es determinar que micro-hbitats favorecen la enfermedad en relacin a la proximidad al bosque, orientacin de las manchas de hongos, distribucin de la enfermedad en las ramas y la presencia de algn cultivo cercano a la planta en estudio. Se determin que hay una mayor abundancia de M. citricolor en C. arabica cuando las plantas estn localizadas cerca del bosque, cerca de un cultivo agrcola y cuando se ubican en medio de las ramas de la planta. El estudio adems concluye que la enfermedad se encuentra mayoritariamente de cara al oeste. En general, los factores topogrficos y ambientales que producen bajas condiciones de luz tienen un efecto significativo en el desarrollo de M. citricolor, entendiendo el impacto de estos factores, los agricultores estn mejor informados en el tipo de micro-hbitat que son ms favorables para la produccin del caf y la reduccin en la transmisin de enfermedades.
Text in English.
Coffee--Diseases and pests
Caf-Enfermedades y plagas
Tropical Ecology Fall 2010
Ecologa Tropical Otoo 2010
t Monteverde Institute : Tropical Ecology
Influence of microhabitat con ditions on the abundance of American Leaf Spot Disease ( Mycena citricolor ) on Coffea arabica Elizabeth Peterson Department of Biology, Denison University ABSTRACT Coffea arabica (Rubiaceae ) is extremely important to the agri culture, economy, and culture of Costa Rica. The yields high amounts of coffee, it also fosters conditions that are optimal for the growth of dis eases, such as Mycena citricolor . This study aimed to determine which microhabitat conditions favor the growth of the disease. In addition to proximity to forest, the orientation of fungi spots, placement of the disease on the branches, and presence of a n agricultural crop near the plant was recorded . It was determined that there was a greater M. citricolor abundance on C. arabica when plants were located closer to the forest, closer to an agricultural crop , and when it resided on the middle branches of the plant . The study also concluded that the disease prefers westerly facing slopes. On a whole, topographical and environmental factors that produce low light conditions have a significant effect on the development of M. citricolor ; in understanding the impact of these characteristics, farmers are better informed on what microhabitats are most suitable for high coffee production and low disease transmission yields . RESUMEN Coffea arabica (Rubiaceae) es sumamente importante para la agricultura, economÃ a y cultura de Costa Rica. La producciÃ³n primaria de cafÃ© se centra en mÃ©todos de cultivo bajo sombra; aunque este mÃ©todo aumenta la producciÃ³n de cafÃ©, tambiÃ©n fomenta condiciones que son Ã³ptimas para el crecimiento de enfermedades como Mycena citricolor . El objetivo de este estudio es determinar que micro hÃ¡bitats favorecen la enfermedad en relaciÃ³n a la proximidad al bosque, orientaciÃ³n de los manchas de hongos, distribuciÃ³n de la enfermedad en las ramas y la presencia de algÃºn cultivo cercano a la plan ta en estudio. Se determiÃ³ que hay una mayor abundancia de M. citricolor en C. arabica cuando las plantas estÃ¡n localizadas cerca del bosque, cerca de un cultivo agrÃcola y cuanod se ubican en las ramas medias de la planta. El estudio ademÃ¡s concluye tam biÃ©n que la enfermedad se encuentra mayoritariamente de cara al oeste. En general, factores topogrÃ¡ficos y ambientales que producen bajas condiciones de luz tienen un efecto significativo en el desarrollo de M. citricolor , entendiendo el impacto de estos factores, los agricultores estÃ¡n mejor informados en el tipo de micro hÃ¡bitat que son mÃ¡s favorables para la producciÃ³n de cafÃ© y reducciÃ³n en la transimisiÃ³n de enfermedades. INTRODUCTION Since its introduction in the late eighteenth century, Coffea arab ica (Rubiaceae) has become an integral component of the c ulture and economy of Costa Rica (Perfecto et al. 1996). The use of important export crop to blossom into a main source of revenue for the count ry ( Muschler 2009 ). In shade dominated management method s , coffee plants are given the opportunity to discourage weed growth, increase pollination likelihood, and have exposure to nutrients from leaf litter (Staver et al. 2001). However, in exchange for low light conditions, coupled with high humidity levels, encourage the development of diseases on coffee plants ( Mouen Bedimo et al. 2008 ).
Depending upon the production environment and management practices that are implemented on a coffee plantation, different fungal pathogens may devel op. For instance, diseases such as leaf rust ( Hemileia vastatrix; Uredinales ; Chaconiaceae) and berry borer ( Hypothenemus hampeii; Coleoptera ; Scolytidae ) are limited by shaded conditions, while the development of American leaf spot disease ( Mycena citric olor; Agaricales ; Mycenaceae ) flourishes under shade (Avelino et al. 2007). M. citricolor , commonly referred to in Central prospers during the rainy season, at moderate levels of humidity, and at middle elevations that contain s hade ( Staver et al. 2001) . Since it thrives in the same plants leaves, branche s, and berries is fairly common throughout coffee plantations in Costa Rica (Staver et al. 2001). Once infected, plants can experience loss of fruits and the leaves can exhibit light brown, circular spots (Staver et al. 2001). Successful spreading of this disease greatly depends upon the environment and the topographical factors surrounding the coff ee plants ( Muschler 2009 ). Given that the location of M. citricolor within the coffee agroecosystem is strongly influenced by shade, small variations in microhabitat conditions can greatly affect disease abundance ( Muschler 2009 ). For instance, differen ces in light intensity of a specific region can create unique mic rohabitats for the production of coffee. Plants that are located closer to a forest, th us having exposure to low light , are likely to produce a favorable microhabitat for M. citricolor , whil e microhabitats with higher light exposure will likely yield lower abundances of the disease (Avelino et al. 2007 b ) . Likewise, if a crop, such as bananas, is present within a coffee plot, it is likely that this microhabitat will be compatible for high M. citricolor development since the presence of a crop can be an additional source of shade (Avelino et al. 2007 b ) . Consequently, topographical and environmental conditions, as well as crop management practices, are related to the abundance of spots on coffee plants ( Muschler 2009 ). The purpose of this study was to identify factors that influence the presence and profusion of American leaf spot disease on C. arabica trees in the Monteverde region of Costa Rica. The study will foc us on differ ent microhabitats in coffee plantations. I hypothesized that the type of microhabitat surrounding a coffee plant will determine the abundance of M. citricolor on the plant; further, if the characteristics of a microhabitat cause low light conditions, I pr edicted that there was going to be a greater presence of the disease on the C. arabica plants. The findings from this study provide farmers with information on optimal coffee production environments. METHODS Study Sites and Sampling Size This study was conducted from October 28 to November 17 2010 on La Finca de los Vargas, which is a shaded coffee farm between 1200 and 1300 meters elevation in CaÃ±itas, Puntarenas, Costa Rica (Fig 1). The region is classified as a lower montane wet forest by Holdridge (Haber 2000). The total area of th e non organic coffee farm is 5.7 hectares, surrounded by 8 hectares of seconda r y forest fragment (Thompson 2010) . The farm primarily produces its coffee ( Coffea a rabica ) using non shaded monoculture practices (95%), howe ver some coffee is produced using commercial polyculture practices (5%) (Thompson 2010) . For the purpo se of this study, only
one plot was used. Also, due to large amounts of rainfall during September, the plants in this plot were treated with Trichoderma (Hypocreales ; Hypocreaceae ). Within the one plot, 90 plants were surveyed for the presence of American leaf s pot forest, two to five meters from a forest, or five to ten meters from a forest. Within each region, t here were at total of 30 plants 15 of which were located underneath a banana or orange tree and the remaining 15 were located 2 meters or more away from a banana or orange tree. In all the region s, t he height of the plants ranged from 1.4 meters to 2.0 meters. Using a counter, the total number of M. citricolor spots per plant was determined. Observations and recordings were made on the total number of spots, most infected region of the plant, and fungi placement in relation to the height. F ungi spots on the leaves were categorized as residing on the l ower, middle, or upper branches; the branch sections were of equal size and were one third of the plants total height. Compass readings of the ori entation of the most infected section of the plant wer e recorded as north, northeast, east, southeast, south, southwest, or w est. FIGURE 1. Map of farm where study was con ducted in Ca Ã± itas, Puntarenas, Costa Rica. The plot that was used is identified wi thin the parameters of the box. RESULTS Fungal distribution in relation to distance and proximity to an agricultural crop Mycena citricolor abundance on C. arabica w as significantly impacted by distance to a forest and proximity to an agricultural crop ( Two Way ANOVA, F = 12 .2 , df = 7,82, p < 0.0001 ; Fig
2 ). The lowest abundance of M. citricolor was present within the five to ten meter range. Distance from forest had a negative effect on M. citricolor abundance: as distance from the forest increased, M . citricolor abundance decreased (One Way ANOVA, F = 28. 3 , df = 2,87, p < 0.0001) . Likewise, proximity to an agricultural crop had a positive influence on M. citricolor (One Way ANOVA, F = 8. 8 , df = 2,87, p < 0.0003 ). Microhabitats that included bananas yielded the highest abundance of M. citricolor spots; the highest abundance of spots, at 563 spots, was on a plant located under a banana tree while the lowest abundance of spots, at 39 spots, was on a plant located under an orange tree. Fungal distrib ution in relation to distance and branch region The branch location, combined with distance from a forest, significantly impacted the percent of M. citricolor spots (Two Way ANOVA, F = 25.2, df = 8,261, p < 0.0001 ; Fig 3 ). T he development of M. citricolo r is most abundant on the middle branches of C. arabica plants (One Way ANOVA, F = 89.2, df = 2,267, p < 0.0001) . The highest mean percent M. citricolor abundance was present amongst the middle branches , with 45.1%, in comparison to 33.3 % on the lower br anches and just 21.5% on the upper branches (Fig 3). Yet proportionally, the most infected branch region on the plant was not significantly impacted by distance from a forest. Fungal distribution in relation slope orientation M ycena citricolor prefers westerly facing slopes and did not grow well in easterly facing slopes (Fig 4). More specifically, 78.8% of the plants most infected regions were orientated towards the northwest, west, or southwest, compared to just 1% being orientated towards the north and 0% of sampled plants most infected region were oriented towards the east.
FIGURE 2. The effect of variations in microhabitats , distance from a forest (less then two meters, between two and five meters, and five to ten meters) and proximity to an agricultural crop (banana, orange, or none) , on the total abundance of M. citricolor spots on a coffee plant. Plant s closer to the forest yielded higher amounts of M. citricolor (ANOVA, p < 0.0001); similarly, coffee plants in close proximity to banan as yielded higher amounts of the disease (ANOVA p<0.0003). FIGURE 3. The effect of distance from a forest and branch location on total p roportion of M. citricolor spots on a coffee plant . There was no relationship between distance from a forest and loc ation on the coffee plant however, across all distances, M. citricolor prefers the middle region of the plant (ANOVA, p < 0.0001).
FIGURE 4. While M. citricolor develops the best when oriented towards westerly facing slopes, the disease did not grow well in easterly facing slopes. This trend can be applied to all distance regions from the forest (less then two meters, between two and five meters, and five to ten meters ). DISCUSSION This study tested further the importance of microhabitat condit ions on the development and abundance of American leaf s pot disease in coffee plantations. One of the most influential topographical factors on M ycena citricolor abundance is distance from a forest. The disease yielded higher abundances when it was close r to a forest because there was less exposure to sunlight in these regions. Since forest species can inhibit sunlight f rom reaching coffee plants , M. citricolor will be more likely to favor plants located underneath these trees (Avelino et al. 2007b). Co nversely, microhabitats that were located at a distance of five to ten meters from a forest exhibited lower amounts of the disease because they were exposed to more direct sunlight. Given that plants within t he five to ten meter region are usually located in the center of a coffee plot, there is a lower likelihood that forest species will inhibit sunlight from reaching these plants. Overall, t he effect of distance on M. citricolor abundance can also be interpreted in amount of light exposure; t he farther the distance a microhabitat is from a patch of forest, the less conducive the environment is to M. citricolor development due to lower amounts of shading from forest species . The abundance of M. citricolor on C. arabica plants was also significantly affec ted by another microhabitat feature, proximity to an agricultural crop. While microhabitats that
included bananas yielded the highest abundance of M. citricolor spots, microhabitats that included oranges or no crops yielded significantly lower abundances of spots. It is likely that the difference between banana, orange, and no crop regions are attributed to the amount of shade produced by each. Since microhabitats with bananas had the most M. citricolor , it is likely these microhabitats are the most favo rable to the development o f the disease because their leaves cast high amounts of shade onto the coffee plants that grow under them ( Avelino et al. 2007b). Additionally, since the leaves of banana trees are oriented in a downward direction, more shade is cast directly onto the leaves of coffee plants. It is also interesting to observe that there is little variation in disease abundance between the orange and no crop microhabitats; t his lack of difference could be attributed to the fact that no orange tree s were present in the zero to two meters region; as a result, it appears as though orange trees in coffee plantations do not impact M. citricolor development as much as the presence of other agricultural crops may, when in fact, they could greatly impact t he disease . In terms of placement on a plant, high concentrations of M. citricolor are significantly dependent upon branch location . In my findings, the distribution of M. citricolor wa s most abundant on the middle branches of a C. arabica plant and le ast present on the upper portions of the plant. High concentrations in the middle branches can be attributed to higher levels of self shading and shading from neighboring trees (Avelino et al. 2007b) . R egard less of a plants height , self shading is most l ikely to occur throughout the middle sections of coffee plants because leaves at this region are the most likely to interact with the leaves of other plants; consequently, higher interaction occurrences at a plants middle section increases the chance of di sea se transmission between plants. Given that the lower branches of a plant extend farther out under the plant, these branches are prone to some degree of self shading but can also be exposed to more direct sunlight; as a result, development of the diseas e can be less predominant on lower branches since it can be impacted by higher light intensities. Seeing as the upper branches of the plant receive the most sunlight, and have the lowest amount of leaves, this region experiences the lowest abundance of M. citricolor (Avelino et al. 2007b). It is also important to recognize that , proportionally, the most infe cted branch region was not significantly impacted by distance from a forest. All three distance regions exhibited highest abundance on their middle b ranches, suggesting that the branch region M. citricolor affects is not dependent on distance from a forest. Since t he fungus developed well in areas that were oriented towards the west , this suggests that these slopes receive less exposure to sunlight; th us , there are higher successful disease transmission rates in these regions due to increased shade coverage , which allows the leaves to remain wetter for longer periods of time (Avelino et al. 2007b). By retaining higher levels of moisture on the leaves, and growing within low light conditions, M. citricolor is more susceptible to development and growth in westerly facing slopes . Conversely, easterly facing slopes were not conducive to M. citricolor development because plants on these slopes experienced m ore exposure to sunlight, thus lower abundance s of the disease (Avelino et al. 2007b). Based on the results, I can conclude that topographical factors that produce low light conditions have a significa nt effect on the development of M. citricolor . Future investigations, for this study, could focus on other topographical and environmental characteristics of coffee microhabitats. More specifically, data could be collected on factors such as amount of light exposure , height of surrounding coffee plants, and distance from other coffee plants. Also, using these topographical and environmental factors, the productivity of coffee plants could be measured; for instance, a further investigation could look at the affect of microhabitat
characteristics on the amoun t of coffee produced from plants within these microhabitats. Lastly, in hopes of uncovering more information o n diseases that affect coffee production, investigations could examine the abundance of other coffee diseases, such as leaf rust and berry borer, on the leaves of coffee plants that are also impacted by M. citricolor ; by noting the presence of other diseases, a better understanding of disease interactions and resulting abundances can be obtained, which can be turned into economical gains by the far mers. ACKNOWLEDGMENTS I would like to thank my advisor Pablo Allen for advising me throughout the duration of my project and for helping me find my study site. I would also like to thank him for helping me analyze my data, perform the necessary statisti cal tests, and creating the needed graphs in Excel. Additionally, I would like to thank Guillermo Vargas and la Finca de Vargas for allowing my to use their farm and for providing me with the background information on their farm. LITERATURE CITED Ave lino, J, H. Zelaya, A. Merlo, A. Pineda, M. OrdoÃ±ez, B. Barboza, M. Barquero, R. Alfaro, C. Esquivel, S. Savary, S. Cabut, J.F. Durand, and C. Cilas. 2007a. Shade effects on two coffee diseases: leaf rust ( Hemileia vastatrix ) and American leaf spot ( Mycen a citricolor ) . International Symposium on Multi Strata Agroforestry Systems with Perennial Crops: Making Ecosystem Services Count for Farmers, Consumers and the Environment. 2:10. Avelino, J., S. Cabut, B. Barboza, M. Barquero, R. Alfaro, C. Esquivel, J.F . Durand, and C. Cilas. 2007b. Topography and crop management are key factors for the development of American leaf spot epidemics on coffee in Costa Rica. Phytopathology 97:1532 1542. Haber, W. 2000. Plant and Vegetation. In: Monteverde Ecology and Cons ervation of a Tropical Cloud Forest, N. M. Nadkarni & N.T. Wheelwright ed. Oxford: 43 44. Looby, C, 2008. Distribution of American Leaf Spot disease ( Mycena citricolor ) in coffee plantations in CaÃ±itas, Costa Rica, CIEE Spring Tropical Ecology and Conse rvation. Mouen Bedimo , J.A., I. Njiayouom , D. Bieysse , M. NdoumbÃ¨ Nkeng , C. Cilas , and J. L. NottÃ©ghem . 2008. Effect of Shade on Arabica Coffee Berry Disease Development: Toward an Agroforestry System to Reduce Disease Impact. Phytopathology 98: 1320 1325. Muschler, R. G. 2009. Shade Management and its Effect on Coffee Growth and Quali ty. In: Coffee: Growing, Processing, Sustainable Production: A Guidebook for Growers, Processors,Traders, and Researchers. J.W. Wintgens , ed. Wiley VHC , Switzerland, pp. 395 424. Perfecto, I. R. A. Rice, R. Greenberg, and M. E. van der Voort. 1996. Shad e Coffee: A Disappearing Refuge for Biodiversity. BioScience 46: 598 608. Staver, C., F. Guharay, D. Monterroso, and R.G. Muschler. 2001. Designing pest suppressive multistrata perennial crop systems: shade grown coffee in Central America. Agroforestry S ystems 53: 151 170. Thompson, K. 2010 . Shade Coffee Farms as Conservation Tools: A Measure of Butterfly Diversity in Coffee Agro ecosystems in the Monteverde Region of Costa Rica . CIEE Spring Tropical Ecology and Conservation.