Can debarking affects sex ratio, population structure and spatial segregation?: insights of unsustainable harvesting in a Mesoamerican tropical tree
Visualizações: 781DOI:
https://doi.org/10.15451/ec2024-01-13.08-1-23Keywords:
Sex ratio, cuachalalate, medicinal bark, population structure, Ripley's K function, spatial pattern, seasonally dry tropical forestAbstract
The ecological mechanisms that contribute to maintaining plant populations have been exhaustively examined around the world, but the relative quantification of the effect of anthropogenic processes on these mechanisms in tropical dioecious tree species has not been revealed yet. The aim of this study was to analyze the effect of debarking on the sex ratio, population structure, distribution and spatial correlation between the sexes and growth stages of Amphipterygium adstringens (Anaciardiaceae), a dioecious tree species that is highly exploited for its medicinal bark. We found differences in plant density between harvested and non-harvested stands. The sex ratio was 1.33♂:1♀ in harvested stands while the opposite was true for non-harvested stands (1.27♀:1♂), which suggest that selective debarking drives androic-skewed and has an impact on reproductive performance. However, despite the dominance of a certain sex in the relative frequencies under each condition, we did not register spatial sex segregation since the analysis suggests that the spatial independence pattern does not differ between sites. In contrast, facilitation requirements (spatial attraction) between androic plants and seedlings, and between seedlings and saplings were found in non-harvested areas, while spatial uniformity patterns on a population level suggest strategies to avoid competition over space and finite resources in stressful environments. These novel findings point out that debarking constitutes a factor that not only modifies the spatial and population structure of a Mesoamerican tropical tree, but it can also influence sex ratio, consequently affecting the long-term conservation of A. adstringens stands.
Downloads
References
Álvarez-Cansino L, Zunzunegui M, Díaz-Barradas M, Correia O, Paz M (2013) Effects of temperature and rainfall variation on population structure and sexual dimorphism across the geographical range of a dioecious species. Population Ecology 55:135–146. DOI: https://doi.org/10.1007/s10144-012-0336-3
Baldauf C, dos Santos F (2014) The effect of management systems and ecosystem types on bark regeneration in Himatanthus drasticus (Apocynaceae): recommendations for sustainable harvesting. Environmental Monitoring and Assessment 186:349–359. DOI: https://doi.org/10.1007/s10661-013-3378-x
Baldauf C, Dias A, Corrêa C, Santos F (2021) Bark harvesting by human population shapes tree allometry in an economically important species of the Brazilian savanna. Forest Ecology and Management 496:119465. DOI: https://doi.org/10.1016/j.foreco.2021.119465
Barret CH, Hough J (2013) Sexual dimorphism in flowering plants. Journal of Experimental Botany 64:67–82. DOI: https://doi.org/10.1093/jxb/ers308
Beltrán-Rodríguez L, Manzo-Ramos F, Maldonado-Almanza B, Martínez-Ballesté A, Blancas J (2017) Wild Medicinal Species Traded in the Balsas Basin, Mexico: Risk Analysis and Recommendations for Their Conservation. Journal of Ethnobiology 37:743–764. DOI: https://doi.org/10.2993/0278-0771-37.4.743
Beltrán-Rodríguez L (2018). Structure, population dynamics and bark regeneration of Amphipterygium adstringens (Anacardiaceae) in Ejido El Limón, Cuauchichinola, Morelos, México. PhD Thesis, Postgrado en Ciencias Forestales, Colegio de Postgraduados, México.
Beltrán-Rodríguez L, Valdez-Hernández J, Luna-Cavazos M, Romero-Manzanares A, Pineda-Herrera E, Maldonado-Almanza B, Borja de la Rosa Ma, Blancas J (2018) Structure and tree diversity of secondary dry tropical forests in the Sierra de Huautla Biosphere Reserve, Morelos. Revista Mexicana de Biodiversidad 89:108–122. DOI: https://doi.org/10.22201/ib.20078706e.2018.1.2004
Beltrán-Rodríguez L, Cristians S, Bye R, Sierra-Huelsz A, Blancas J, Maldonado-Almanza B (2020) Barks as non-timber forest products in Mexico: National analysis and recommendations for their sustainable use. Instituto de Biología, Universidad Nacional Autónoma de México, México.
Beltrán-Rodríguez L, Valdez-Hernández JI, Saynes-Vásquez A, Blancas J, Sierra-Huelsz JA, Cristians S, Martínez-Ballesté A, Romero-Manzanares A, Luna-Cavazos M, Borja de la Rosa MA, Pineda-Herrera E, Maldonado-Almanza B, Ángeles-Pérez G, Ticktin T, Bye R (2021) Sustaining Medicinal Barks: Survival and Bark Regeneration of Amphipterygium adstringens (Anacardiaceae), a Tropical Tree under Experimental Debarking. Sustainability 13:2860. DOI: https://doi.org/10.3390/su13052860
Beltrán-Rodríguez L, Ticktin T, Martínez-Ballesté A, Romero-Manzanares A, Valdez-Hernández J, Cruz-Rodríguez J, Bye R, Blancas J (2022a) Effects of habitat disturbance and rainfall on a dominant medicinal dry forest tree. Forest Ecology and Management 520:120362. DOI: https://doi.org/10.1016/j.foreco.2022.120362
Beltrán-Rodríguez L, Romero-Manzanares A, Borja de la Rosa Ma, Valdéz-Hernández J, Luna-Cavazos M, Blancas J (2022b) Adaptive advantages of wood anatomical–hydraulic features linked to sex in a tropical dioecious species. Trees 36:39-52. DOI: https://doi.org/10.1007/s00468-021-02258-w
Beltrán-Rodríguez L, Bye R (2023) Amphipterygium adstringens (Schltdl.) Standl. Amphipterygium glaucum (Hemsl. & Rose) Hemsl. & Rose Amphipterygium molle (Hemsl.) Hemsl. & Rose Amphipterygium simplicifolium (Standl.) Cuev. ANACARDIACEAE. In: Casas A, Blancas-Vázquez JJ (eds) Ethnobotany of the Mountain Regions of Mexico. Ethnobotany of Mountain Regions. Springer, Cham. México, pp. 1067–1080. DOI: https://doi.org/10.1007/978-3-030-99357-3_28
Besag J (1977) Contribution to the discussion on Dr. Ripley’s paper. Journal of the Royal Statistical Society Series B Statistical Methodology 39:193–195. DOI: https://doi.org/10.1111/j.2517-6161.1977.tb01628.x
Besag J, Diggle PJ (1977) Simple Monte Carlo tests for spatial pattern. Journal of the Royal Statistical Society Series C Applied Statistics 26:327–333. DOI: https://doi.org/10.2307/2346974
Bierzychudek P, Eckhart V (1988) Spatial segregation of the sexes of dioecious plants. The American Naturalist 132:34–43. DOI: https://doi.org/10.1086/284836
Botha J, Witkowski E, Shackleton C (2014) Harvesting impacts on commonly used medicinal tree species (Catha edulis and Rapanea melanophloeos) under different land management regimes in the Mpumalanga Lowveld, South Africa. Koedoe 47:1–18. DOI: https://doi.org/10.4102/koedoe.v47i2.77
Bonduriansky R (2007) The genetic architecture of sexual dimorphism: the potential roles of genomic imprinting and condition dependence. In: Fairbairn DJ, Blanckenhorn WU, Székely T. (eds). Sex, Size, and Gender Roles Evolutionary Studies of Sexual Size Dimorphism. Oxford UP, New York, pp. 176–184. DOI: https://doi.org/10.1093/acprof:oso/9780199208784.003.0020
Bram MR, Quinn JA (2000) Sex expression, sex-specific traits, and the effects of salinity on growth and reproduction of Amaranthus cannabinus (Amaranthaceae), a dioecious annual. American Journal of Botany 87:1609–1618. DOI: https://doi.org/10.2307/2656737
Coelho P, Ferreira P, de Paiva E, Apgaua E, Madeira B, de Oliveira G, Ferrerira Y, Santoa R, Tng D (2017) Tree succession across a seasonally dry tropical forest and forest-savanna ecotone in northern Minas Gerais, Brazil. Journal of Plant Ecology 10:859–868. DOI: https://doi.org/10.1093/jpe/rtw091
Condit R, Ashton PS, Baker P, Bunyavejchewin S, Gunatilleke S, Gunatilleke N, Hubbell SP, Foster RB, Itoh A, Lafrankie J V, Lee HS, Losos E, Manokaran N, Sukumar R, Yamakur T (2000) Spatial patterns in the distribution of tropical tree species. Science 288: 1414–1418. DOI: https://doi.org/10.1126/science.288.5470.1414
Cox PA (1981) Niche partitioning between sexes of dioecious plants. The American Naturalist 117:295–307. DOI: https://doi.org/10.1086/283707
Cuevas X (2005) A revision of the genus Amphipterygium (Julianiaceae). Ibugana 13:27–47.
da Silva J, da Silva L, Albuquerque, U, Cardoso C (2018) Bark and latex harvesting short-term impact on native tree species reproduction. Environmental Monitoring and Assessment 190:744. DOI: https://doi.org/10.1007/s10661-018-7081-9
Dale M R, Fortin MJ (2014) Spatial Analysis: A Guide for Ecologists. Cambridge University Press, Cambridge, USA. DOI: https://doi.org/10.1017/CBO9780511978913
Dawson TE, Ehleringer JR (1993) Gender specific physiology, carbon isotope discrimination, and habitat distribution in box-elder, Acer negundo. Ecology 74:798–815. DOI: https://doi.org/10.2307/1940807
Dawson TE, Geber MA (1999) Sexual dimorphism in physiology and morphology. In: Geber MA, Dawson TE, Delph LF (eds.) Gender and sexual dimorphism in flowering plants. Springer-Verlag, Berlin, Heidelberg, pp. 176–215. DOI: https://doi.org/10.1007/978-3-662-03908-3_7
Delph LF (1999) Sexual dimorphism in life history. In: Geber MA, Dawson TE, Delph LF (eds) Gender and sexual dimorphism in flowering plants. Springer-Verlag Berlin, Heidelberg, pp. 149–173. DOI: https://doi.org/10.1007/978-3-662-03908-3_6
Diggle PJ (1983) Statistical Analysis of Spatial Point Patterns. Academic Press.
Djoudi H, Vergles E, Blackie RR, KoffiKoame C, Gautier D (2015) Dry forests, livelihoods and poverty alleviation: understanding current trends. International Forestry Review 17:54–69. DOI: https://doi.org/10.1505/146554815815834868
Dudley LS, Galen C (2007) Stage-dependent patterns of drought tolerance and gas exchange vary between sexes in the alpine willow, Salix glauca. Oecologia 153:1–9. DOI: https://doi.org/10.1007/s00442-007-0712-4
Field DL. Pickup M, and Barrett CH (2013a) Ecological context and metapopulation dynamics affect sex‐ratio variation among dioecious plant populations. Annals of Botany 111:917–923. DOI: https://doi.org/10.1093/aob/mct040
Field DL, Pickup M, Barrett CH (2013b) Comparative analyses of sex‐ratio variation in dioecious flowering plants. Evolution 67:661–672. DOI: https://doi.org/10.1111/evo.12001
Fisher M (2000) Toolbox: Software available for sophisticated spatial statistics. [Computer software]. University of the South Pacific, Suva, Fiji.
Forero-Montaña J, Zimmerman JK, Thompson J (2010) Population structure, growth rates and spatial distribution of two dioecious tree species in a wet forest in Puerto Rico. Journal of Tropical Ecology 26:433–443. DOI: https://doi.org/10.1017/S0266467410000143
Freckleton R, Silva D, Bovi M, Watkinson AR (2003) Predicting the impacts of harvesting using structured populations models: the importance of density-dependence and timing of harvested for a tropical palm tree. Journal of Applied Ecology 40:846–858. DOI: https://doi.org/10.1046/j.1365-2664.2003.00842.x
Freeman DC, Klikoff LG, Harper KT (1976) Differential resource utilization by the sexes of dioecious plants. Science 193:597–599. DOI: https://doi.org/10.1126/science.193.4253.597
Gaoue O, Ticktin T (2007) Patterns of harvesting foliage and bark from the multipurpose tree Khaya senegalensis in Benin: Variation across ecological regions and its impacts on population structure. Biological Conservation 137:424–436. DOI: https://doi.org/10.1016/j.biocon.2007.02.020
García E (2004) Modificaciones al Sistema de Clasificación Climática de Köppen (para adaptarlo a las condiciones de la República Mexicana). Instituto de Geografía, Universidad Nacional Autónoma de México, México.
Geber MA, Dawson TE, Delph LF (1999) Gender and sexual dimorphism in flowering plants. Springer-Verlag, Berlin, Heidelberg. DOI: https://doi.org/10.1007/978-3-662-03908-3
Hernández F 1959. Historia Natural de Nueva España. Tomo I, II y III. Universidad Nacional Autónoma de México, México.
Hernández-Barrios J, Niels PR, Ackerly D, Martínez-Ramos M (2012) Defoliation and gender effects on fitness components in three congeneric and sympatric understorey palms. Journal of Ecology 100:1544–1556. DOI: https://doi.org/10.1111/j.1365-2745.2012.02011.x
Hersch-Martínez P (1999) Destino común: Los recolectores y su flora medicinal. El comercio de flora medicinal silvestre desde el suroccidente poblano. Instituto Nacional de Antropología e Historia, México.
Hidalgo-Contreras E (2019) Ecology of the dispersal of Amphipterygium adstringens (Schltdl.) Standl. (Anacardiaceae) in secondary deciduous tropical forests of Morelos: silvicultural bases for its management. BSc thesis, Faculty of Biology, Universidad Autónoma del Estado de Morelos, México.
Hubbell SP (1979) Tree dispersion, abundance, and diversity in a tropical dry forest. Science 203:1299–1309. DOI: https://doi.org/10.1126/science.203.4387.1299
Infante-Gil S, Zárate de Lara GP (2010) Métodos estadísticos. Un enfoque interdisciplinario. Trillas, México.
Jansen M, Anten NP, Bongers F, Martínez‐Ramos M, Zuidema P (2018) Towards smarter harvesting from natural palm populations by sparing the individuals that contribute most to population growth or productivity. Journal of Applied Ecology 55:1682–1691. DOI: https://doi.org/10.1111/1365-2664.13100
Kang H, Shin S (2012) Sex ratios and spatial structure of the dioecious tree Torreya nucifera in Jeju Island, Korea. Journal of Ecology and Field Biology 35:111–122. DOI: https://doi.org/10.5141/JEFB.2012.015
Laloo RC, Kharlukhi L, Jeeva S, Mishra BP (2006) Status of medicinal plants in the disturbed and the undisturbed sacred forests of Meghalaya, northeast India: population structure and regeneration efficacy of some important species. Current Science 90:225–232.
Lanuza O, Casanoves F, Vílches-Mendoza S, Espelta J, Peñuelas J, Peguero G (2023) Structure, diversity and the conservation value of tropical dry forests in highly fragmented landscapes. Journal of Plant Ecology 16:rtac046. DOI: https://doi.org/10.1093/jpe/rtac046
Lloyd DG, Webb CJ (1977) Secondary sex characters in plants. The Botanical Review 43:177–216. DOI: https://doi.org/10.1007/BF02860717
López-Zariñana M (2023). Potencial reproductivo de Amphipterygium adstringens (Anacardiaceae) en dos condiciones de manejo del Bosque Tropical Caducifolio secundario en Morelos. BSc thesis, Faculty of Sciences, Universidad Autónoma del Estado de Morelos, México.
Lotwick HW, Silverman BW (1982) Methods for analysing spatial processes of several types of points. Journal of the Royal Statistical Society, Series B (Statistical Methodology) 44:406–413. DOI: https://doi.org/10.1111/j.2517-6161.1982.tb01221.x
Luna-Nieves AL, Meave JA, Cerdeira LP, Ibarra-Manríquez G (2017) Reproductive phenology of useful seasonally dry tropical forest trees: guiding patterns for seed collection and plant propagation in nurseries. Forest Ecology and Management, 393:52–62. DOI: https://doi.org/10.1016/j.foreco.2017.03.014
McDonald MA, McLaren KP, Newton AC (2010) What are the mechanisms of regeneration post-disturbance in tropical dry forest?. (CEE review 07-013 -SR37- Environmental Evidence). Bangor University, Wales, UK.
McKown AD, Klápště J, Guy RD, Soolanayakanahally RY, Mantia J, Porth I, Skyba O, Unda F, Douglas CJ, El-Kassaby YA, Hamelin RC, Mansfield SD, Cronk QC (2017) Sexual homomorphism in dioecious trees: extensive tests fail to detect sexual dimorphism in Populus. Nature 7:1–14. DOI: https://doi.org/10.1038/s41598-017-01893-z
Méndez-Toribio M. González-Di Pierro AM, Quesada M, Benítez-Malvido J (2014) Regeneration beneath a dioecious tree species (Spondias purpurea) in a Mexican tropical dry forest. Journal of Tropical Ecology 30:265–268. DOI: https://doi.org/10.1017/S0266467414000066
Muller-Landau H, Hardesty B (2005) Seed dispersal of woddy species plants in tropical forest: concepts, examples and future directions. In: Burslem DF, Pinard MA, Hartley SE (eds) Biotic interactions in the tropics: their role in maintenance of species diversity. Cambridge University Press, UK, pp. 267–309. DOI: https://doi.org/10.1017/CBO9780511541971.012
Munné-Bosch S (2015) Sex ratios in dioecious plants in the framework of global change. Environmental and Experimental Botany 109:99–102. DOI: https://doi.org/10.1016/j.envexpbot.2014.08.007
Navarrete A, Mata R (2009) Medicinal plants of Mexico. Scientific monograph. Quality control tests (identification and composition), efficacy and safety. Cuachalalate Amphipterygium adstringens (Schltdl.) Standl. (Anacardiaceae). Sentido Giratorio Ediciones, México.
Newton P, Peres A, Desmoulière S, Watkinson A (2012) Cross-scale variation in the density and spatial distribution of an Amazonian non-timber forest resource. Forest Ecology and Management 276:41–51. DOI: https://doi.org/10.1016/j.foreco.2012.03.020
Nicotra AB (1998) Sex ratio variation and spatial distribution of Siparuna grandiflora, a tropical dioecious shrub. Oecologia 115:102–113. DOI: https://doi.org/10.1007/s004420050496
Niklas KJ (1997) The Evolutionary Biology of Plants. University of Chicago Press, USA.
Nuñez CI, Nuñez MA, Kitzberger T (2008) Sex-related spatial segregation and growth in a dioecious conifer along environmental gradients in northwestern Patagonia. Ecoscience 15:73–80. DOI: https://doi.org/10.2980/1195-6860(2008)15[73:SSSAGI]2.0.CO;2
Obeso JR (2002) The costs of reproduction in plants. New Phytologist 155:321–348. DOI: https://doi.org/10.1046/j.1469-8137.2002.00477.x
Opler P, Bawa K (1978) Sex ratios in tropical forest trees. Evolution 32:812–821. DOI: https://doi.org/10.1111/j.1558-5646.1978.tb04636.x
Oke T (1987) Boundary Layer Climates (2nd ed.). Taylor & Francis, Routledge.
Ortiz P, Arista M, Talavera S (2002) Sex ratio and reproductive effort in the dioecious Juniperus communis subsp. alpina (Suter) Celak (Cupressaceae) along an altitudinal gradient. Annals of Botany 89:205–211. DOI: https://doi.org/10.1093/aob/mcf028
Ortega-Baranda V, De la Cruz-Salinas DL, Romero-Manzanares A, Sánchez-Bernal EI (2023). Estructura poblacional y fenología de cuachalalate (Amphipterygium adstringens) desarrollado sobre litosol degradado en la costa de Oaxaca. Terra Latinoamericana 41:1–16. DOI: https://doi.org/10.28940/terra.v41i0.1595
Oviedo-Chavez I, Ramírez-Apan TR, Soto-Hernández M, Martínez-Vázquez M (2004) Principles of the bark of Amphipterygium adstringens (Julianaceae) with anti-inflammatory activity. Phytomedicine 11:436–445. DOI: https://doi.org/10.1016/j.phymed.2003.05.003
Pacini E, Nepi M (2007) Nectar production and presentation. In: Nicolson S, Nepi M, Pacini E (eds) Nectaries and nectar. Springer, Dordrecht, the Netherlands, pp 167–21. DOI: https://doi.org/10.1007/978-1-4020-5937-7_4
Pittermann J (2010) The evolution of water transport in plants: an integrated approach. Geobiology 8:112–139. DOI: https://doi.org/10.1111/j.1472-4669.2010.00232.x
Poorter L, McDonald I, Alarcón A, Fichtler E, Licona JC, Peña-Claros M, Sterck F, Villegas Z, Sass-Klaassen U (2009) The importance of wood traits and hydraulic conductance for the performance and life history strategies of 42 rainforest tree species. New Phytologist 185:481–92. DOI: https://doi.org/10.1111/j.1469-8137.2009.03092.x
Pyke G (1991) What does it cost a plant to produce floral nectar?. Nature 350: 58–59. DOI: https://doi.org/10.1038/350058a0
Queenborough SA, Burslem D, Garwood C, Valencia R (2007) Neighborhood and community interactions determine the spatial pattern of tropical tree seedling survival. Ecology 88:224–2258. DOI: https://doi.org/10.1890/06-0737.1
Quesada M, Rosas F, Aguilar R, Ashworth L, Rosas-Guerrero VM, Sayago R, Lobo JA, Herrerías-Diego Y, Sánchez-Montoya G (2011) Human Impacts on Pollination, Reproduction, and Breeding Systems in Tropical Forest Plants. In Dirzo R., Young HS, Mooney H, Ceballos G (eds) Seasonally Dry Tropical Forests. Ecology and Conservation, Island Press, Washington, DC, pp. 173–194. DOI: https://doi.org/10.5822/978-1-61091-021-7_11
R Development Core Team (2023). R package. [https://www.r-project.org/] Accessed 28 April 2023.
Ramos-Ordoñez MF, Santamaría-Estrada LR, Gonzalez-López TG, Isidra-Flores K, Contrera-González AM (2022). Parámetros poblacionales de una especie medicinal en riesgo, el caso de Amphipterygium adstringens. Revista Mexicana de Biodiversidad 93: 1–21. DOI: https://doi.org/10.22201/ib.20078706e.2022.93.3908
Réjou-Méchain M, Flores O, Bourland N, Doucet JL, Fétéké RF, Pasquier A, Hardy O (2011) Spatial aggregation of tropical trees at multiple spatial scales. Journal of Ecology 99:1373–1381.
Rhen T (2007) Sex differences: genetic, physiological, and ecological mechanisms. In: Fairbairn DJ, Blanckenhorn WU, Székely T. (eds). Sex, Size, and Gender Roles Evolutionary Studies of Sexual Size Dimorphism. Oxford UP, New York, pp. 166–175. DOI: https://doi.org/10.1093/acprof:oso/9780199208784.003.0019
Réjou-Méchain M, Flores O, Bourland N, Doucet JL, Fétéké RF, Pasquier A, Hardy O (2011) Spatial aggregation of tropical trees at multiple spatial scales. Journal of Ecology 99:1373–1381. DOI: https://doi.org/10.1111/j.1365-2745.2011.01873.x
Rincón E, Huante P (1993) Growth responses of tropical deciduous tree seedlings to contrasting light conditions. Trees 7:202–207. DOI: https://doi.org/10.1007/BF00202074
Ripley BD 1977 Modeling spatial patterns (with discussion). Journal of the Royal Statistical Society Series B (Statistical Methodology) 39:172–212. DOI: https://doi.org/10.1111/j.2517-6161.1977.tb01615.x
Rodríguez T (2003) Management and conservation of commercial medicinal plants in the municipality of Copalillo, Guerrero. Master thesis, Faculty of Sciences, Universidad Nacional Autónoma de México, México.
Ruiz J, Fandiño M, Chazdon R (2005) Vegetation structure, composition, and species richness across a 56‐year chronosequence of dry tropical forest on Providencia Island, Colombia. Biotropica 37:520–30. DOI: https://doi.org/10.1111/j.1744-7429.2005.00070.x
Roland N, Loh E, Enow E, Bechem E, Yengo T (2013) Spatial distribution and abundance of selected exploited non-timber forest products in the Takamanda National Park, Cameroon. International Journal of Biodiversity and Conservation 5:378–388.
Romero C (2014) Bark: Structure and Functional Ecology. Advances in Economic Botany 17:5–26.
Romero-Manzanares A, Beltrán-Rodríguez L, Valdez-Hernández J. (2016). Population structure and spatial correlation between sexes and stages of development in Amphipterygium adstringens (Anacardiaceae). [Paper presentation]. Memories of the XX Mexican Congress of Botany, Abstract OR7 Functional Ecology. Botanical Society of Mexico, Mexico City, Mexico.
Savi MK, Noumonvi R, Chadaré FJ, Daïnou K, Salako VK, Idohou R, Assogbadjo AE, Kakaï RG (2018) Synergy between traditional knowledge of use and tree population structure for sustainability of Cola nitida (Vent.) Schott. and Endl in Benin (West Africa). Environment, Development and Sustainability 21:1357–1368. DOI: https://doi.org/10.1007/s10668-018-0091-5
Schumann K, Wittig R, Thiombiano A, Becker U, Hahn K (2011) Impact of land-use type and harvesting on population structure of a non-timber forest product-providing tree in a semi-arid savanna, West Africa. Biological Conservation 144:2369–2376. DOI: https://doi.org/10.1016/j.biocon.2011.06.018
Seidler TG, Plotkin JB (2006) Seed dispersal and spatial patterns in tropical trees. PLoS Biology 4:2132–2137. DOI: https://doi.org/10.1371/journal.pbio.0040344
Servicio Meteorologico Nacional (2010) Normales Climatológicas por Estado. Comisión Nacional del Agua. [https://smn.conagua.gob.mx/es/informacion-climatologica-por-estado?estado=mor] (accessed 16 Dec 2022).
Sinclair JP, Emlen J, Freeman D (2012) Biased sex ratios in plants: Theory and trends. The Botanical Review 78:63–86. DOI: https://doi.org/10.1007/s12229-011-9065-0
Sotelo-Barrera M, Cília-García M, Luna-Cavazos M, Díaz-Núñez JL, Romero-Manzanares A, Soto-Hernández RM, Castillo-Juárez I (2022) Amphipterygium adstringens (Schltdl.) Schiede ex Standl (Anacardiaceae): An Endemic Plant with Relevant Pharmacological Properties. Plants 11:1766. DOI: https://doi.org/10.3390/plants11131766
Stockdale M, López-Binnqüist C (2019) Manejo comunitario sustentable de Productos Forestales No Maderables. Un manual para América Latina. Programa de Intercambio de Productos Forestales No Maderables para el sur y sureste de Asia (NTFP-EP), Centro de Investigaciones Tropicales de la Universidad Veracruzana (CITRO-UV), Red Temática Conacyt “Productos Forestales No Maderables: aportes desde la etnobiología para su aprovechamiento sostenible” (Red-PFNM), and People and Plants International, México.
Szmyt J (2014) Spatial statistics in ecological analysis: from indices to functions. Silva Fennica 48:1–31. DOI: https://doi.org/10.14214/sf.1008
Thomas SC (1997) Geographic parthenogenesis in a tropical forest tree. American Journal of Botany 84:1012–1015. DOI: https://doi.org/10.2307/2446292
Ticktin T, Ganesan R, Paramesh M (2012) Disentangling the effects of multiple anthropogenic drivers on the decline of two tropical dry forest trees. Journal of Applied Ecology 49:774-784. DOI: https://doi.org/10.1111/j.1365-2664.2012.02156.x
van Lent J, Hernández-Barrios JC, Anten NP, Martínez-Ramos M (2014) Defoliation effects on seed dispersal and seedling recruitment in a tropical rain forest understorey palm. Journal of Ecology 102:709–720. DOI: https://doi.org/10.1111/1365-2745.12216
Varghese A, Ticktin T, Mandle L (2015) Importance of, and approach for, assessing the effects of multiple stressors on the regeneration of fruit harvested trees in a tropical dry forest. PLoS One 10:e0119634. DOI: https://doi.org/10.1371/journal.pone.0119634
Vásquez-Cortez VF, Beltrán-Rodríguez L, Ángeles-Pérez G, Romero-Manzanares A, Garcia-Moya E, Luna-Cavazos M, Caballero J, Blancas J, Martínez-Ballesté A, Montoya-Reyes F (2020) ¿El descortezamiento de un árbol medicinal impacta en su estructura poblacional-espacial? El caso de Hintonia latiflora en México. Madera y Bosques 26:e2622037. DOI: https://doi.org/10.21829/myb.2020.2622037
Vedel-Sørensen MJ, Tovaranonte P, Bøcher H, Balslev, Barfod AS (2013) Spatial distribution and environmental preferences of 10 economically important forest palms in western South America. Forest Ecology and Management 307:284–292. DOI: https://doi.org/10.1016/j.foreco.2013.07.005
Velázquez E, Martínez I, Getzin S, Moloney KA, Wiegand T (2016) An evaluation of the state of spatial point pattern analysis in ecology. Ecography 39:1–14. DOI: https://doi.org/10.1111/ecog.01579
Verdú M, García-Fayos P (1998) Female biased sex ratios in Pistacia lentiscus L. (Anacardiaceae). Plant Ecology 135:95–101. DOI: https://doi.org/10.1023/A:1009764613803
Vieira DL, Scariot A (2006) Principles of Natural Regeneration of Tropical Dry Forests for Restoration. Restoration Ecology 14:11–20. DOI: https://doi.org/10.1111/j.1526-100X.2006.00100.x
Wilson K, Hardy IC (2002) Statistical analysis of sex ratios: an introduction. In: Hardy IC (ed) Sex ratios: concepts and research methods. Cambridge University Press, UK, pp. 48–92. DOI: https://doi.org/10.1017/CBO9780511542053.004
Wright SJ, Kitajima K, Kraft NJ, Reich PB, Wright IJ, Bunker DE, Condit R, Dalling JW, Davies SJ, Díaz S, Engelbrecht BM, Harms KE, Hubbell SP, Marks CO, Ruiz-Jaen MC, Salvador CM, Zanne AE (2010) Functional traits and the growth–mortality trade-off in tropical trees. Ecology 91:3664–3674. DOI: https://doi.org/10.1890/09-2335.1
Zanne AE, Falster D (2010) Plant functional traits - Linkages among stem anatomy, plant performance and life history. New Phytologist 185:348–51. DOI: https://doi.org/10.1111/j.1469-8137.2009.03135.x
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Leonardo Beltrán, Angélica Romero-Manzanares, Tamara Ticktin, José Blancas, Andrea Martínez Ballesté, Orou Gaoue, Robert Bye
This work is licensed under a Creative Commons Attribution 4.0 International License.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
