Shade coffee farms promote genetic diversity of native trees

Abstract

Coffee is cultivated across 11 million hectares (ha) of land within the world's richest centers of terrestrial biodiversity [1Myers N. Mittermeier R.A. Mittermeier C.G. da Fonseca G.A.B. Kent J. Biodiversity hotspots for conservation priorities.Nature. 2000; 403: 853-858Crossref PubMed Scopus (17418) Google Scholar]. In tropical America, coffee is traditionally grown under a diverse canopy of overstory shade trees, which enhances the quality of the coffee farm as a conservation matrix and supports a broad spectrum of pollinators that increase fruit set per bush [2Perfecto I. Rice R.A. Greenberg R. VanderVoort M.E. Shade coffee: A disappearing refuge for biodiversity.Bioscience. 1996; 46: 598-608Crossref Scopus (637) Google Scholar, 3Donald P.F. Biodiversity impacts of some agricultural commodity production systems.Conserv. Biol. 2004; 18: 17-37Crossref Scopus (370) Google Scholar, 4Klein A.M. Cunningham S.A. Bos M. Steffan-Dewenter I. Advances in pollination ecology from tropical plantation crops.Ecology. 2008; 89: 935-943Crossref PubMed Scopus (102) Google Scholar]. Unlike sun coffee monocultures, shade coffee also sustains a diverse array of vertebrates, including bats and migratory birds, which provide farmers with many ecological services, such as insect predation [5Williams-Guillen K. Perfecto I. Vandermeer J. Bats limit insects in a neotropical agroforestry system.Science. 2008; 320: 70Crossref PubMed Scopus (176) Google Scholar], and may also conserve seed dispersal processes necessary for native tree re-establishment [6Sekercioglu C.H. Ecological significance of bird populations.in: Del Hoyo J. Elliott A. Christie D. Handbook of the Birds of the World. Volume 11. Barcelona, Lynx Edicions2006: 15-51Google Scholar]. However, little is known about the capacity of shade coffee farms to maintain gene flow and genetic diversity of remnant tree populations across this common tropical landscape. In this study, we conducted genetic analyses that reveal recent colonization and extensive gene flow of a native tree species in shade coffee farms in Chiapas, Mexico. The high genetic diversity and overlapping deme structure of the colonizing trees also show that traditional coffee farms maintain genetic connectivity with adjacent habitats and can serve as foci of forest regeneration. Coffee is cultivated across 11 million hectares (ha) of land within the world's richest centers of terrestrial biodiversity [1Myers N. Mittermeier R.A. Mittermeier C.G. da Fonseca G.A.B. Kent J. Biodiversity hotspots for conservation priorities.Nature. 2000; 403: 853-858Crossref PubMed Scopus (17418) Google Scholar]. In tropical America, coffee is traditionally grown under a diverse canopy of overstory shade trees, which enhances the quality of the coffee farm as a conservation matrix and supports a broad spectrum of pollinators that increase fruit set per bush [2Perfecto I. Rice R.A. Greenberg R. VanderVoort M.E. Shade coffee: A disappearing refuge for biodiversity.Bioscience. 1996; 46: 598-608Crossref Scopus (637) Google Scholar, 3Donald P.F. Biodiversity impacts of some agricultural commodity production systems.Conserv. Biol. 2004; 18: 17-37Crossref Scopus (370) Google Scholar, 4Klein A.M. Cunningham S.A. Bos M. Steffan-Dewenter I. Advances in pollination ecology from tropical plantation crops.Ecology. 2008; 89: 935-943Crossref PubMed Scopus (102) Google Scholar]. Unlike sun coffee monocultures, shade coffee also sustains a diverse array of vertebrates, including bats and migratory birds, which provide farmers with many ecological services, such as insect predation [5Williams-Guillen K. Perfecto I. Vandermeer J. Bats limit insects in a neotropical agroforestry system.Science. 2008; 320: 70Crossref PubMed Scopus (176) Google Scholar], and may also conserve seed dispersal processes necessary for native tree re-establishment [6Sekercioglu C.H. Ecological significance of bird populations.in: Del Hoyo J. Elliott A. Christie D. Handbook of the Birds of the World. Volume 11. Barcelona, Lynx Edicions2006: 15-51Google Scholar]. However, little is known about the capacity of shade coffee farms to maintain gene flow and genetic diversity of remnant tree populations across this common tropical landscape. In this study, we conducted genetic analyses that reveal recent colonization and extensive gene flow of a native tree species in shade coffee farms in Chiapas, Mexico. The high genetic diversity and overlapping deme structure of the colonizing trees also show that traditional coffee farms maintain genetic connectivity with adjacent habitats and can serve as foci of forest regeneration. Previous genetic studies of forest regeneration in degraded tropical landscapes have focused on canopy trees and have found pronounced fine-scale spatial genetic structure within colonizing tree populations (e.g., [7Sezen U.U. Chazdon R.L. Holsinger K.E. Genetic consequences of tropical second-growth forest regeneration.Science. 2005; 307: 891Crossref PubMed Scopus (81) Google Scholar, 8Aldrich P.R. Hamrick J.L. Reproductive dominance of pasture trees in a fragmented tropical forest mosaic.Science. 1998; 281: 103-105Crossref PubMed Scopus (239) Google Scholar]) as a result of limited seed dispersal from scattered maternal trees. Such population bottlenecks can lead to inbreeding depression and demographic declines for plants in fragmented landscapes. Alternatively, agricultural matrices that facilitate the movement of seed and pollen dispersers among habitats can increase the breeding size and genetic diversity of native plant populations. We used genetic markers to analyze the dispersal history and spatial genetic structure of the understory tree Miconia affinis (Melastomataceae) within a network of coffee farms and forest fragments in Chiapas, Mexico. Though an integral part of tropical forests, relatively little is known about the population genetics of understory trees compared with canopy trees. Like many tropical understory trees, the seeds of the genus Miconia are dispersed by widespread large-bodied birds, such as the clay-colored thrush (Turdus grayi), as well as small-bodied scrub and forest specialists such as the chestnut-sided warbler (Dendroica pensylvanica) [9Luck G.W. Daily G.C. Tropical countryside bird assemblages: Richness, composition, and foraging differ by landscape context.Ecol. Appl. 2003; 13: 235-247Crossref Scopus (164) Google Scholar]; thus, its colonization patterns are likely representative of other understory vertebrate-dispersed trees. M. affinis is an obligate outcrosser and requires native bees (e.g., Trigona and Scaptotrigona spp.) for cross-fertilization through buzz-pollination, of which the ubiquitous Africanized honeybees are incapable. The survey area of 1,200 ha encompasses an uncut primary forest and three adjacent shade coffee farms (Figure 1). The three farms were clear-cut and burned in the late 1930s and immediately replanted with coffee bushes and canopy tree species, including nitrogen-fixing legumes and many other fruit trees (means of 157.21 ha−1 overstory trees, and 14.67 ha−1 tree species). Since the creation of these coffee farms, farmers have allowed native understory trees, like M. affinis, to colonize the coffee plots because they help to reduce soil erosion. Strong spatial genetic structure of M. affinis found in the forest plots (Sp statistic = 0.020) is similar to levels reported in species with extreme seed dispersal limitation [10Vekemans X. Hardy O.J. New insights from fine-scale spatial genetic structure analyses in plant populations.Mol. Ecol. 2004; 13: 921-935Crossref PubMed Scopus (890) Google Scholar]; in contrast, no spatial genetic structure was detected for any distance class within the coffee farms (Sp statistic = 0.006), revealing more extensive gene flow across the shade coffee matrix (Figure 1). Limited seed dispersal in the forest, relative to the coffee farm, may be due to the short foraging ranges of forest specialist birds. Using an individual-based clustering approach, M. affinis individuals in the landscape were assigned to four well-supported demes (96% posterior probability), which were overlapping in space and not aggregated by habitat or age class, indicating that colonization into the farms was recent and from multiple source populations (Figure 1 and Table S1) [7Sezen U.U. Chazdon R.L. Holsinger K.E. Genetic consequences of tropical second-growth forest regeneration.Science. 2005; 307: 891Crossref PubMed Scopus (81) Google Scholar]. Levels of M. affinis genetic diversity within the coffee farms did not differ from forest populations [7Sezen U.U. Chazdon R.L. Holsinger K.E. Genetic consequences of tropical second-growth forest regeneration.Science. 2005; 307: 891Crossref PubMed Scopus (81) Google Scholar]. These results depart from previous agricultural colonization studies that report strong spatial genetic structure and reduced genetic diversity in the founding canopy tree populations, usually caused by the reproductive dominance of just a few maternal trees in the early colonizing stages [7Sezen U.U. Chazdon R.L. Holsinger K.E. Genetic consequences of tropical second-growth forest regeneration.Science. 2005; 307: 891Crossref PubMed Scopus (81) Google Scholar]. By conserving resident bird populations, our results reveal that shade coffee farms support extensive dispersal processes crucial for the connectivity of remnant forest and agricultural habitats. The colonization pattern and high genetic diversity of M. affinis also points to the role of shade coffee farms as potential foci of native forest regeneration, as coffee farms typically fall out of production in less than a century. However, despite the clear ecological benefits of traditional shade coffee farms, these farms are rapidly being converted to input-intensive monocultures [2Perfecto I. Rice R.A. Greenberg R. VanderVoort M.E. Shade coffee: A disappearing refuge for biodiversity.Bioscience. 1996; 46: 598-608Crossref Scopus (637) Google Scholar, 3Donald P.F. Biodiversity impacts of some agricultural commodity production systems.Conserv. Biol. 2004; 18: 17-37Crossref Scopus (370) Google Scholar]. Thus, it is imperative to highlight the ecological function of shade coffee farms, not only in providing refuge for native fauna, but also in preserving habitat connectivity and gene-flow processes essential for reforestation by native tree species. This project was supported by the Helen Olson Brower Fellowship at the University of Michigan (to S.J.) and the National Science Foundation (award DEB 043665 to C.W.D.). The authors would like to thank John Vandermeer for help in the development and implementation of this project. The authors would also like to thank the farmers in Nueva Alemania, Chiapas for the permission to collect samples on their land. Download .pdf (.02 MB) Help with pdf files Document S1. Supplemental Experimental Procedures, Supplemental References, and One Table