Shade coffee plantations maintain woody plant diversity and structure in a cloud forest landscape of southern Mexico

Abstract

Cloud forest ecosystems of the Latin American tropics are highly threatened by changes in land-use such as expanding croplands and livestock pastures that promote shifts in the structure and composition of plant communities in these forests. However, shade coffee plantations represent a forest management alternative that has been shown to maintain biodiversity in these ecosystems. In this study, we evaluated changes in the composition, diversity, and structure of Mexican cloud-forest woody species for three land use categories: cattle pastures, shade coffee plantations and advanced succession forests. For each category, fifteen 0.28-ha plots were established and the composition and diversity of vegetation was noted. Composition of species was analyzed using ordination methods, and alpha diversity was compared using Hill numbers. Seventy-seven woody species belonging to 40 families were recorded. Species richness and diversity was high in both the advanced successional forest and coffee plantations compared to cattle pastures. Vegetation composition and structure was similar between late succession forests and coffee plantations with both land uses also being more structurally complex than cattle pastures. Our results show how shade coffee cultivation is a land-use activity that maintains woody plant communities in a manner that aligns with biodiversity conservation.

Keywords

Land uses / Late succession / Plant diversity / Shade coffee / Vegetation structure

References

[1] Almazán-Núñez RC, Corcuera P, Parra-Juárez L, Jiménez-Hernández J, Charre GM. Changes in structure and diversity of woody plants in a secondary mixed pine-oak in the Sierra Madre del Sur of Mexico. Forests, 2016 7 4 90

[2] Almazán-Núñez RC, Charre GM, Pineda-López R, Corcuera P, Rodríguez-Godínez R, Alvarez-Alvarez EA, Bahena-Méndez A. dos Santos-Viana HF, García-Morote FA. Relationship between bird diversity and habitat along a pine-oak successional forest in southern Mexico. New perspectives in forest science, 2018, London, UK: IntechOpen 185 201

[3] Almeda F. Rzedowski J, Rzedowski GC. Melastomataceae. Flora del bajío y regiones adyacentes. Fascículo 10, 1993, Veracruz: Instituto de Ecología AC 1 36

[4] APG IV (Angiosperm Phylogeny Group). An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc, 2016, 181(1): 1-20.

[5] Avelino J, Cristancho M, Georgiou S, Imbach P, Aguilar L, Bornemann G, Läderach P, Anzueto F, Hruska AJ, Morales C. The coffee rust crises in Colombia and Central America (2008–2013): impacts, plausible causes and proposed solutions. Food Secur, 2015, 7(2): 303-321.

[6] Bagella S, Caria MC, Farris E, Rossetti I, Filigheddu R. Traditional land uses enhanced plant biodiversity in a Mediterranean agro-silvo-pastoral system. Plant Biosyst, 2016, 150(2): 201-207.

[7] Bandeira FP, Martorell C, Meave JA, Caballero J. The role of rustic coffee plantations in the conservation of wild tree diversity in the Chinantec region of Mexico. Biodivers Conserv, 2005, 14(5): 1225-1240.

[8] Carvajal S, González-Villarreal LM. La familia Cecropiaceae en el estado de Jalisco, Mexico, 2005, Jalisco: Universidad de Guadalajara 25

[9] Chao A, Jost L. Estimating diversity and entropy profiles via discovery rates of new species. Methods Ecol Evol, 2015, 6(8): 873-882.

[10] Chao A, Ma KH, Hsieh TC (2016). iNEXT (iNterpolation and EXTrapolation) online: software for interpolation and extrapolation of species diversity. https://chao.shinyapps.io/iNEXTOnline/. Accessed 15 Oct 2019

[11] Clarke KR. Non-parametric multivariate analyses of changes in community structure. Aust J Ecol, 1993, 18(1): 117-143.

[12] Colwell RK (2013) EstimateS: statistical estimation of species richness and shared species from samples. Version 9.1.0. Storrs, USA: University of Connecticut. http://viceroy.eeb.uconn.edu/estimates/index.html. Accessed 15 Oct 2019

[13] Colwell RK, Coddington JA. Estimating terrestrial biodiversity through extrapolation. Philos Trans R Soc B, 1994, 345(1311): 101-118.

[14] Cubiña A, Aide TM. The effect of distance from forest edge on seed rain and soil seed bank in a tropical pasture. Biotropica, 2001, 33(2): 260-267.

[15] Dávalos-Sotelo R, Morato MI, Pinillos-Cueto EM. Manson RH, Hernández-Ortiz V, Gallina S, Mehltreter K. Almacenamiento de carbono. Agroecosistemas cafetaleros de Veracruz: biodiversidad, manejo y conservación, 2008, Mexico: Instituto de Ecología AC-Instituto Nacional de Ecología 223 234

[16] Davidson S. Shade coffee agro-ecosystems in Mexico. J Sustain For, 2004, 21(1): 81-95.

[17] de Leeuw J, Mair P. Multidimensional scaling using majorization: SMACOF in R. J Stat Softw, 2009, 31(3): 1-30.

[18] DeClerck FAJ, Chazdon R, Holl KD, Milder JC, Finegan B, Martinez-Salinas A, Imbach P, Canet L, Ramos Z. Biodiversity conservation in human-modified landscapes of Mesoamerica: past, present and future. Biol Conserv, 2010, 143(10): 2301-2313.

[19] Díaz S, Lavorel S, McIntyre S, Falczuk V, Casanoves F, Milchunas DG, Skarpe C, Rusch G, Sternberg M, Noy-Meir I, Landsberg J, Zhang W, Clark H, Campbell BD. Plant trait responses to grazing—a global synthesis. Glob Chang Biol, 2007, 13: 313-341.

[20] Fjeldså J, Burgess ND. The coincidence of biodiversity patterns and human settlement in Africa. Afr J Ecol, 2008, 46(1): 33-42.

[21] García CM, Guevara-Féver F, Rodríguez MAM, Silva-Sáenz P, Chávez-Carbajal MA, García-Ruíz I. Estudio florístico en el área de la comunidad indígena de Nuevo San Juan Parangaricutiro, Michoacán, México. Acta Bot Mex, 2000, 52: 5-41.

[22] Geissert D, Ibáñez A. Manson RH, Hernández-Ortiz V, Gallina S, Mehltreter K. Calidad y ambiente físicoquímico de los suelos. Agroecosistemas cafetaleros de Veracruz: biodiversidad, manejo y conservación, 2008, México: Instituto de Ecología AC-Instituto Nacional de Ecología 213 222

[23] González-Zamora A, Esperón-Rodríguez M, Barradas VL. Mountain cloud forest and grown-shade coffee plantations: a comparison of tree biodiversity in central Veracruz, Mexico. For Syst, 2016, 25(1): 1-11.

[24] Gresser C, Tickell S. Mugged: poverty in your cup, 2002, Washington: Oxfam International 54

[25] Gual-Díaz M, Rendón-Correa A. Bosques mesófilos de montaña de México: diversidad, ecología y manejo, 2014, Mexico: Comisión Nacional para el Conocimiento y Uso de la Biodiversidad 351

[26] Hamilton LS, Juvik JO, Scatena FN. Tropical montane cloud forest, 1995, New York: Springer 352

[27] Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Version 2.17. Norway: University of Oslo. https://palaeo-electronica.org/2001_1/past/issue1_01.htm. Accessed 15 Oct 2019

[28] Hernández-Ladrón IG, Rojas-Soto OR, López-Barrera F, Puebla-Olivares F, Díaz-Castelazo C. Dispersión de semillas por aves en un paisaje de bosque mesófilo en el centro de Veracruz, México: su papel en la restauración pasiva. Rev Chil Hist Nat, 2012, 85(1): 89-100.

[29] Holl KD, Loik ME, Lin EHV, Samuels IA. Tropical montane forest restoration in Costa Rica: overcoming barriers to dispersal and establishment. Restor Ecol, 2000, 8(4): 339-349.

[30] Hooper E, Legendre P, Condit R. Barriers to forest regeneration of deforested and abandoned land in Panama. J Appl Ecol, 2005, 42(6): 1165-1174.

[31] Hortal J, Borges PA, Gaspar C. Evaluating the performance of species richness estimators: sensitivity to simple grain size. J Anim Ecol, 2006, 75(1): 274-287.

[32] INEGI (2010) (Instituto Nacional de Estadística, Geografía e Informática). Página electrónica institucional. https://www.inegi.org.mx/. Accessed 15 Oct 2019

[33] IUSS Working Group WRB (2015) Base referencial mundial del recurso suelo 2014, actualización 2015: sistema internacional de clasificación de suelos para la nomenclatura de suelos y la creación de leyendas de mapas de suelos. Informes sobre recursos mundiales de suelos 106. FAO, Roma, Italia, p 218

[34] Jackson D, Skillman J, Vandermeer J. Indirect biological control of the coffee leaf rust, Hemileia vastatrix, by the entomogenous fungus Lecanicillium lecanii in a complex coffee agroecosystem. Biol Control, 2012, 61: 89-97.

[35] Jose S. Agroforestry for conserving and enhancing biodiversity. Agrofor Syst, 2012, 85(1): 1-8.

[36] Jost L. Entropy and diversity. Oikos, 2006, 113(2): 363-375.

[37] Juárez-Lopez BM, Velázquez-Rosas N, López-Binnqüist C. Tree diversity and uses in coffee plantations of a Mixe community in Oaxaca, Mexico. J Ethnobiol, 2017, 37(4): 765-778.

[38] Kelaidis P. Bone M, Johnson D, Kelaidis P, Kintgen M, Vickerman LG. Introduction: principal steppe regions. Steppes: the plants and ecology of the world’s semiarid regions, 2015, Portland: Timber Press 360

[39] Kikoti IA, Mligo C. Impacts of livestock grazing on plant species composition in montane forests on the northern slope of Mount Kilimanjaro, Tanzania. Int J Biodivers Sci Ecosyst Serv Manag, 2015, 11(2): 114-127.

[40] Lambin E, Turner B, Geist H, Agbola S, Angelsen A, Bruce J, Coomes O, Dirzo R, Fischer G, Folke C, George P, Homewood K, Imbernon J, Leemans R, Li X, Moran E, Mortimore M, Ramakrishnan P, Richards J, Skanes H, Steffen W, Stone G, Svedin U, Veldkamp T, Vogel C, Xu J. The causes of land-use and land-cover change: moving beyond the myths. Glob Environ Chang, 2001, 11(4): 261-269.

[41] Legendre P, Gallagher E. Ecologically meaningful transformations for ordination of species data. Oecologia, 2001, 129: 271-280.

[42] López-Barrera F, Landgrave R. Manson RH, Hernández-Ortiz V, Gallina S, Mehltreter K. Variación de la biodiversidad a nivel paisaje. Agroecosistemas cafetaleros de Veracruz: biodiversidad, manejo y conservación, 2008, Mexico: Instituto de Ecología AC-Instituto Nacional de Ecología 259 270

[43] López-Gómez AM, Williams-Linera G, Manson RH. Tree species diversity and vegetation structure in shade coffee farms in Veracruz, Mexico. Agric Ecosyst Environ, 2008, 124: 160-172.

[44] López-Mata L, Villaseñor JL, Cruz-Cárdenas G, Ortiz E, Ortiz-Solorio C. Predictores ambientales de la riqueza de especies de plantas del bosque húmedo de montaña de México. Bot Sci, 2012, 90(1): 27-36.

[45] Lozada T, de Koning GHJ, Marché R, Klein A-M, Tscharntke T. Tree recovery and seed dispersal by birds: comparing forests, agroforestry and abandoned agroforestry in coastal Ecuador. Perspect Plant Ecol Evol Syst, 2007, 8(3): 131-140.

[46] Lugo A, Herlmer E. Emerging forests on abandoned land: Puerto Rico’s new forests. For Ecol Manag, 2004, 190: 145-161.

[47] Luna-Vega I, Espinosa D, Contreras-Medina R. Biodiversidad de la Sierra Madre del Sur: una síntesis preliminar, 2016, Mexico: Universidad Nacional Autónoma de México 528

[48] MacGregor-Fors I, Payton ME. Contrasting diversity values: statistical inferences based on overlapping confidence intervals. PLoS ONE, 2013 8 2 e56794

[49] Macip-Ríos R, Casas-Andreu G. Los cafetales en México y su importancia para la conservación de los anfibios y reptiles. Acta Zool Mex, 2008, 24(2): 143-159.

[50] Manson RH, Hernández-Ortiz V, Gallina S, Mehltreter K. Agroecosistemas cafetaleros de Veracruz: biodiversidad, manejo y conservación, 2008, Mexico: Instituto de Ecología AC-Instituto Nacional de Ecología 348

[51] Marcano-Vega H, Aide TH, Báez D. Forest regeneration in abandoned coffee plantations and pastures in the cordillera central of Puerto Rico. Plant Ecol, 2002, 161(1): 75-87.

[52] Martínez ML, Pérez-Maqueo O, Vázquez G, Castillo-Campos G, García-Franco J, Mehltreter K, Equihua M, Landgrave R. Effects of land use change on biodiversity and ecosystem services in tropical montane cloud forests of Mexico. For Ecol Manag, 2009, 258(9): 1856-1863.

[53] Martini AMZ, dos Santos FAM. Effects of distinct types of disturbance on seed rain in the Atlantic forest of NE Brazil. Plant Ecol, 2007, 190(1): 81-95.

[54] Méndez VE, Gliessman SR, Gilbert GS. Tree biodiversity in farmer cooperatives of a shade coffee landscape in western El Salvador. Agric Ecosyst Environ, 2007, 119: 145-159.

[55] Mendoza-Ponce A, Corona-Núñez R, Kraxner F, Leduc S, Patrizio P. Identifying effects of land use cover changes and climate change on terrestrial ecosystems and carbon stocks in Mexico. Glob Environ Chang, 2018, 53: 12-23.

[56] Meylan L, Gary C, Allinne C, Ortiz J, Jackson L, Rapidel B. Evaluating the effect of shade trees on provision of ecosystem services in intensively managed coffee plantations. Agric Ecosyst Environ, 2017, 245: 32-42.

[57] Miceli-Méndez CL, Ferguson BG, Ramírez-Marcial N. Myster RW. Seed dispersal by cattle: natural history and applications to Neotropical forest restoration and agroforestry. Post-agricultural succession in the Neotropics, 2008, New York: Springer 165 191

[58] Minchin P. An evaluation of the relative robustness of techniques for ecological ordination. Vegetation, 1987, 69: 89-107.

[59] Moguel P, Toledo VM. Biodiversity conservation in traditional coffee systems of Mexico: a review. Conserv Biol, 1999, 13(1): 1-11.

[60] Montaña C, Ezcurra E. Simple instrument for quick measurement of crown projections. J For, 1980, 78: 699.

[61] Muller-Dombois D, Ellenberg H. Aims and methods of vegetation ecology, 1974, New York: Wiley 580

[62] Muñiz-Castro MA, Williams-Linera G, Benayas JM. Distance effect from cloud forest fragments on plant community structure in abandoned pastures in Veracruz, Mexico. J Trop Ecol, 2006, 22(4): 431-440.

[63] Orlóci L. Multivariate analysis in vegetation research, 1978, Basel: Springer 452

[64] Ortega-Pieck A, López-Barrera F, Ramírez-Marcial N, García-Franco JG. Early seedling establishment of two tropical montane cloud forest tree species: the role of native and exotic grasses. For Ecol Manag, 2011, 261(7): 1336-1343.

[65] Pascarella JB, Aide TM, Serrano MI, Zimmerman JK. Land-use history and forest regeneration in the Cayey Mountains, Puerto Rico. Ecosystems, 2000, 3(3): 217-228.

[66] Perfecto I, Vandermeer J. Quality of agroecological matrix in a tropical montane landscape: ants in coffee plantations in southern Mexico. Conserv Biol, 2002, 16(1): 174-182.

[67] Perfecto I, Rice RA, Greenberg R, van der Voort ME. Shade coffee: a disappearing refuge for biodiversity. Bioscience, 1996, 46(8): 598-608.

[68] Perfecto I, Vandermeer J, Mas A, Soto-Pinto L. Biodiversity, yield, and shade coffee certification. Ecol Econ, 2005, 54(4): 435-446.

[69] Perfecto I, Armbrecht I, Philpott SM, Soto-Pinto L, Dietsch TM. Tscharntke T, Leuschner C, Zeller M, Guhadja E, Bidin A. Shaded coffee and the stability of rainforest margins in northern Latin America. The stability of tropical rainforest margins: linking ecological, economic and social constraints of land use and conservation, 2007, Basel: Springer 227 264

[70] Philpott SM, Bichier P, Rice R, Greenberg R. Field-testing ecological and economic benefits of coffee certifications programs. Conserv Biol, 2007, 21(4): 975-985.

[71] Philpott SM, Arendt WJ, Armbrecht I, Bichier P, Diestch TV, Gordon C, Greenberg R, Perfecto I, Reynoso-Santos R, Soto-Pinto L, Tejeda-Cruz C, Williams-Linera G, Valenzuela J, Zolotoff JM. Biodiversity loss in Latin American coffee landscapes: review of the evidence on ants, birds, and trees. Conserv Biol, 2008, 22(5): 1093-1105.

[72] Ponce-Reyes R, Reynoso-Rosales VH, Watson JEM, VanDerWal J, Fuller RA, Pressey RL, Possingham HP. Vulnerability of cloud forest reserves in Mexico to climate change. Nat Clim Chang, 2012, 2: 448-452.

[73] Rahmanian S, Hejda M, Ejtehadi H, Farzam M, Memariani F, Pyšek P. Effects of livestock grazing on soil, plant functional diversity, and ecological traits vary between regions with different climates in northeastern Iran. Ecol Evol, 2019, 9(14): 8225-8237.

[74] Rangel SR, Carlos E, Zenteno R, de Lourdes M, Enriquez A. El género Quercus (Fagaceae) en el estado de Mexico. Ann Mo Bot Gard, 2002, 89(4): 551-593.

[75] Rojas-Soto O, Sosa V, Ornelas JF. Forecasting cloud forest in eastern and southern Mexico: conservation insights under future climate change scenarios. Biodivers Conserv, 2012, 21(10): 2671-2690.

[76] Şekercioğlu CH, Daily GC, Ehrlich PR. Ecosystem consequences of bird declines. Proc Nat Acad Sci USA, 2004, 101(52): 18042-18047.

[77] SEMARNAT (2010) (Secretaría de Medio Ambiente y Recursos Naturales). Norma Oficial Mexicana NOM-059-SEMARNAT-2010, Protección ambiental-Especies nativas de México de flora y fauna silvestres, Categoría de riesgo y especificaciones para su inclusión, exclusión o cambio-Lista de especies en riesgo. Diario Oficial de la Federación, Diciembre 30, 2010. Ciudad de México, México. http://biblioteca.semarnat.gob.mx/janium/Documentos/Ciga/agenda/DOFsr/DO2454.pdf. Accessed 16 Oct 19

[78] Somarriba E. Pasture growth and floristic composition under the shade of guava (Psidium guajava L.) trees in Costa Rica. Agrofor Syst, 1988, 6: 153-162.

[79] Soto-Pinto L, Romero-Alvarado Y, Caballero-Nieto J, Segura G. Woody plant diversity and structure of shade-grown-coffee plantations in Northern Chiapas, Mexico. Rev Biol Trop, 2001, 49: 977-987.

[80] Soto-Pinto L, Villalvazo-Lopez V, Jimenez-Ferrer G, Ramirez-Marcial N, Montoya G, Sinclair F. The role of local knowledge in determining shade composition of multistrata coffee systems in Chiapas, Mexico. Biodivers Conserv, 2007, 16(2): 419-436.

[81] Soto-Pinto L, Castillo-Santiago MA, Jiménez-Ferrer G. Moutinho P. Agroforestry systems and local institutional development for preventing deforestation in Chiapas, Mexico. Deforestation around the world, 2012, London: IntechOpen 333 350

[82] SPSS (2011) SPSS Statistics for Windows. Version 20.0. SPSS Institute Inc, Chicago, USA. https://www.ibm.com/mx-es/analytics/spss-statistics-software. Accessed 15 Oct 19

[83] Staver C, Bustamante O, Siles P, Aguilar C, Quinde K, Castellón J, Somarriba F, Tapia A, Brenes S, Deras M, Matute N. Intercropping bananas with coffee and trees: prototyping agroecological intensification by farmers and scientists. Acta Hortic, 2013, 986: 79-85.

[84] ter Braak CJF, Ŝmilauer P (2002) CANOCO Reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination (version 4.5). Microcomputer Power, Ithaca, New York, USA. www.canoco.com. Accessed 15 Oct 19

[85] Tscharntke T, Clough Y, Bhagwat SA, Buchori D, Faust H, Hertel D, Hölscher D, Juhrbandt J, Kessler M, Perfecto I, Scherber C, Schroth G, Veldkamp E, Wanger TC. Multifunctional shade-tree management in tropical agroforestry landscapes: a review. J Appl Ecol, 2011, 48(3): 619-629.

[86] Vandermeer J, de la Cerda IG. Height dynamics of the thinning canopy of a tropical rain forest: 14 years of succession in a post-hurricane forest in Nicaragua. For Ecol Manag, 2004, 199(1): 125-135.

[87] Vandermeer J, Perfecto I, Liere H. Evidence for hyperparasitism of coffe rust (Hemileia vastatrix) by the entomogeneous fungus, Lecanicillium lecanii, through a complex ecological web. Plant Pathol, 2009, 58(4): 636-641.

[88] Vázquez-Yanez C, Batis-Muñoz AI, Alcocer-Silva MI, Gual-Díaz M, Sánchez-Dirzo C (1999) Árboles y arbustos potencialmente valiosos para la restauración ecológica y la reforestación. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad-Instituto de Ecología AC-Universidad Nacional Autónoma de México, México, DF, p 15

[89] Villaseñor JL (2010) El bosque húmedo de montaña en México y sus plantas vasculares: catálogo florístico-taxonómico. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad-Universidad Nacional Autónoma de México, México, DF, p 38

[90] Villaseñor JL. Checklist of the native vascular plants of Mexico. Rev Mex Biodivers, 2016, 87: 559-902.

[91] W3Tropicos (2010) Missouri Botanical Garden’s VAST nomenclatural database and associated authority files. Missouri Botanical Garden, Saint Louis, Missouri. http://tropicos.org/. Accessed 16 Oct 19

[92] Wendt T. Lot A, Chiang F. Árboles. Manual de herbario: administración y manejo de colecciones, técnicas de recolección y preparación de ejemplares botánicos, 1986, México: Consejo Nacional de la Flora de México AC 133 142

[93] Williams-Linera G, López-Gómez A. Manson RH, Hernández-Ortiz V, Gallina S, Mehltreter K. Estructura y diversidad de la vegetación leñosa. Agroecosistemas cafetaleros de Veracruz: biodiversidad, manejo y conservación, 2008, Mexico: Instituto de Ecología AC-Instituto Nacional de Ecología 55 68

[94] Williams-Linera G, Manson RH, Vera EI. La fragmentación del bosque mesófilo de montaña y patrones de uso del suelo en la región oeste de Xalapa, Veracruz, México. Madera y Bosques, 2002, 8(1): 69-85.

[95] Williams-Linera G, Toledo-Garibaldi M, Hernández CG. How heterogeneous are the cloud forest communities in the mountains of central Veracruz, Mexico?. Plant Ecol, 2013, 214(5): 685-701.

[96] Zdravko B, Shingo N. Abandoned coffee plantations: biodiversity conservation or path for nonnative species? Case study in a Neotropical montane forest. Interciencia, 2014, 39(8): 554-561.