Hostname: page-component-669899f699-7xsfk Total loading time: 0 Render date: 2025-05-04T13:15:01.414Z Has data issue: false hasContentIssue false
  • English
  • Français

Revisiting the phenology of El Triunfo cloud forest, Mexico, 30 years later

Published online by Cambridge University Press:  23 September 2024

Allen Wootton Open the ORCID record for Allen Wootton [Opens in a new window] ,
Paula L. Enríquez ,
Guadalupe Williams-Linera Open the ORCID record for Guadalupe Williams-Linera [Opens in a new window]  and
Esteban Pineda-Diez de Bonilla
Allen Wootton*
Affiliation:
Departamento de Conservación de la Biodiversidad, El Colegio de la Frontera Sur. Carretera Panamericana y Periférico Sur, San Cristóbal de las Casas, Mexico
Paula L. Enríquez
Affiliation:
Departamento de Conservación de la Biodiversidad, El Colegio de la Frontera Sur. Carretera Panamericana y Periférico Sur, San Cristóbal de las Casas, Mexico
Guadalupe Williams-Linera
Affiliation:
Red de Ecología Funcional, Instituto de Ecología, A.C., Xalapa, Mexico
Esteban Pineda-Diez de Bonilla
Affiliation:
Instituto de Ciencias Biológicas, Universidad de Ciencias y Artes de Chiapas. 29035, Tuxtla Gutiérrez, Mexico
*
Corresponding author: Allen Wootton; Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Climatic conditions have changed within the cloud forests of southern Mexico, but the effects of these changes on tree phenology are not well understood. Our study aimed to determine relationships between seasonal patterns of flowering and fruiting and the annual and long-term changes in temperature and rainfall in El Triunfo Biosphere Reserve, Mexico. Flowering and ripe fruiting intensity and fruit number were recorded for 158 trees of 21 zoochorous species during 17 months in 2019–2021. Circular statistics, synchronization calculations, and generalized linear mixed models were used to determine phenological patterns and relationships between phenophases and temperature, rainfall, and solar radiation. Flowering was most closely associated (negatively) with rainfall, whereas ripe fruiting was positively associated with solar radiation. We compared recent fruiting seasonality with phenological data collected in 1991–1993. The mean date of community fruiting in 2019–2020 was earlier (April 4) than in 1992 (May 1) and 1993 (May 13). Community fruit number in 2020–2021 decreased in comparison to 2019–2020. Our results suggest that decadal trends of increasing minimum daily temperature and an earlier and wetter wet season influenced the timing of community fruiting phenology, and fruit numbers varied greatly between years, possibly impacting resource availability for frugivores in El Triunfo.

Keywords

Chiapasclimate changecloud forestfloweringfruitingfrugivores
Type
Research Article
Information
Journal of Tropical Ecology , Volume 40 , 2024 , e18
Check for updates
Copyright
© The Author(s), 2024. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Almorox, J, Bocco, M and Willington, E (2013) Estimation of daily global solar radiation from measured temperatures at Cañada de Luque, Córdoba, Argentina. Renewable Energy 60, 382–387.CrossRefGoogle Scholar
Arnold, K, Gosling, J and Holmes, D (2005) The Java Programming Language. Reading, USA: Addison Wesley Professional.Google Scholar
Ávila, ML, Hernandez, VH and Velarde, E (1996) The diet of resplendent quetzal (Pharomachrus moncinno mocinno: Trogonidae) in a Mexican cloud forest. Biotropica 28, 720–727.Google Scholar
Barnes, J (2015). Phenological and altitudinal changes in plants responding to drying Neotropical Cloud Forests (Bachelor Thesis). Retrieved from University of Colorado, University Libraries. https://scholar.colorado.edu/concern/undergraduate_honors_theses/tb09j621h Google Scholar
Bates, D, Mächler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48. https://doi:10.18637/jss.v067.i01 CrossRefGoogle Scholar
Batschelet, E (1981) Circular Statistics in Biology. New York, NY: Academic Press.Google Scholar
Bendix, J, Homeier, J, Ortiz, EC, Emck, P, Breckle, SW, Richter, M and Beck, E (2006) Seasonality of weather and tree phenology in a tropical evergreen mountain rain forest. International Journal of Biometeorology 50, 370–384. https://doi.org/10.1007/s00484-006-0029-8 CrossRefGoogle Scholar
Borchert, R, Robertson, K, Schwartz, MD and Williams-Linera, G (2005) Phenology of temperate trees in tropical climates. International Journal of Biometeorology 50, 57–65. https://doi.org/10.1007/s00484-005-0261 CrossRefGoogle ScholarPubMed
Boyle, WA (2010) Does food abundance explain altitudinal migration in a tropical frugivorous bird? Canadian Journal of Zoology 88, 204–213. https://doi.org/10.1139/Z09-133 CrossRefGoogle Scholar
Boyle, WA and Bronstein, JL (2012) Phenology of tropical understory trees: patterns and correlates. Revista de Biología Tropical 60, 1415–1430.CrossRefGoogle ScholarPubMed
Breedlove, DE (1981) Flora of Chiapas. Part 1. Introduction to the Flora of Chiapas. San Francisco, USA: California Academy of Sciences.Google Scholar
Brito, VL, Maia, FR, Silveira, FA, Fracasso, CM, Lemos-Filho, JP, Fernandes, GW, Goldenberg, R, Morellato, LPC, Sazima, M and Staggemeier, VG (2017) Reproductive phenology of Melastomataceae species with contrasting reproductive systems: contemporary and historical drivers. Plant Biology 19, 806–817. https://doi.org/10.1111/plb.12591 CrossRefGoogle ScholarPubMed
Bruijnzeel, LA, Mulligan, M and Scatena, FN (2011) Hydrometeorology of tropical montane cloud forests: emerging patterns. Hydrological Processes 25, 465–498. https://doi.org/10.1002/hyp.7974 CrossRefGoogle Scholar
Bustamante, M, Barrios, M and Juárez, D (2010) Fenología de las plantas nutricias del quetzal (Pharomachrus mocinno mocinno de La Llave) y su efecto sobre la abundancia de quetzales en el Biotopo del Quetzal y corredor Biológico del Bosque Nuboso, Baja Verapaz. Informe final de Investigación. Centro de Estudios Conservacionistas – Dirección General de Investigación, Universidad de San Carlos de Guatemala.Google Scholar
Butt, N, Seabrook, L, Maron, M, Law, BS, Dawson, TP, Syktus, J and McAlpine, CA (2015) Cascading effects of climate extremes on vertebrate fauna through changes to low-latitude tree flowering and fruiting phenology. Global Change Biology 21, 3267–3277.CrossRefGoogle ScholarPubMed
Camacho, M and Orozco, L (1998) Patrones fenológicos de doce especies arbóreas del bosque montano de la Cordillera de Talamanca, Costa Rica. Revista de Biología Tropical 46, 533–542.Google Scholar
Chapman, CA, Chapman, LJ, Struhsaker, TT, Zanne, AE, Clark, CJ and Poulsen, JR (2005) A long-term evaluation of fruiting phenology: importance of climate change. Journal of Tropical Ecology 21, 31–45. https://doi.org/10.1017/S0266467404001993 CrossRefGoogle Scholar
Chapman, CA, Valenta, K, Bonnell, TR, Brown, KA and Chapman, LJ (2018) Solar radiation and ENSO predict fruiting phenology patterns in a 15-year record from Kibale National Park, Uganda. Biotropica 50, 384–395. https://doi.org/10.1111/btp.12559 CrossRefGoogle Scholar
CONAGUA (Comisión Nacional del Agua) (2021) Estaciones Meteorológicas Automáticas (EMAS). Available at https://smn.conagua.gob.mx/es/observando-el-tiempo/estaciones-meteorologicas-automaticas-ema-s (accessed 2021 July 20).Google Scholar
Cox, NJ (2004). Circular statistics in Stata, revisited. In Proceedings of the 10th UK Users Group Meeting, London, UK.Google Scholar
de Azevedo, PV, de Souza, CB, da Silva, BB and da Silva, VP (2007) Water requirements of pineapple crop grown in a tropical environment, Brazil. Agricultural Water Management 88, 201–208. https://doi.org/10.1016/j.agwat.2006.10.021 CrossRefGoogle Scholar
Dinerstein, E (1986) Reproductive ecology of fruit bats and the seasonality of fruit production in a Costa Rican cloud forest. Biotropica 18, 307–318.CrossRefGoogle Scholar
Du, Y, Li, D, Yang, X, Peng, D, Tang, X, Liu, H, Li, D, Hong, X and Song, X (2020) Reproductive phenology and its drivers in a tropical rainforest national park in China: implications for Hainan gibbon (Nomascus hainanus) conservation. Global Ecology and Conservation 24, e01317. https://doi.org/10.1016/j.gecco.2020.e01317 CrossRefGoogle Scholar
Dunham, AE, Razafindratsima, OH, Rakotonirina, P and Wright, PC (2018) Fruiting phenology is linked to rainfall variability in a tropical rain forest. Biotropica 50, 396–404. https://doi.org/10.1111/btp.12564 CrossRefGoogle Scholar
Finch, JT, Power, SA, Welbergen, JA and Cook, JM (2021) Staying in touch: how highly specialised moth pollinators track host plant phenology in unpredictable climates. BMC Ecology and Evolution 21, 1–13. https://doi.org/10.1186/s12862-021-01889-4 CrossRefGoogle ScholarPubMed
Fournier, LA (1974) Un método cuantitativo para la medición de características fenológicas en árboles. Turrialba 24, 422–423.Google Scholar
Frankie, GW, Baker, HG and Opler, PA (1974) Comparative phenological studies of trees in tropical wet and dry forests in the lowlands of Costa Rica. The Journal of Ecology 62, 881–919.CrossRefGoogle Scholar
Freitas, L and Bolmgren, K (2008) Synchrony is more than overlap: measuring phenological synchronization considering time length and intensity. Brazilian Journal of Botany 31, 721–724. https://doi.org/10.1590/S0100-84042008000400017 CrossRefGoogle Scholar
Fuentes-Franco, R, Coppola, E, Giorgi, F, Pavia, EG, Diro, GT and Graef, F (2015) Inter-annual variability of precipitation over Southern Mexico and Central America and its relationship to sea surface temperature from a set of future projections from CMIP5 GCMs and RegCM4 CORDEX simulations. Climate Dynamics 45, 425–440. https://doi.org/10.1007/s00382-014-2258-6 CrossRefGoogle Scholar
Giambelluca, TW, DeLay, JK, Nullet, MA, Scholl, MA and Gingerich, SB (2011) Canopy water balance of windward and leeward Hawaiian cloud forests on Haleakalā, Maui, Hawai’i. Hydrological Processes 25, 438–447. https://doi.org/10.1002/hyp.7738 CrossRefGoogle Scholar
Gómez de Silva, H, González-García, F and Casillas-Trejo, MP (1999) Birds of the upper cloud forest of El Triunfo, Chiapas, Mexico. Ornitologia Neotropical 10, 1–26.Google Scholar
González-Espinosa, M, Meave, JA, Lorea-Hernández, FG, Ibarra-Manríquez, G and Newton, AC (2011) The Red List of Mexican Cloud Forest Trees. Cambridge, UK: Fauna & Flora International. http://www.globaltrees.org/rl_mexican_cloudforest.htm Google Scholar
González-García, F, Santana-C, E, Barbudo, PDJ, Rico-Gray, V and Moliner, VU (2017) Diet and feeding behavior of the Horned Guan (Oreophasis derbianus) in Mexico. The Wilson Journal of Ornithology 129, 771–782. https://doi.org/10.1676/16-041.1 CrossRefGoogle Scholar
González-Zamora, A, Arroyo-Rodríguez, V, Chaves, ÓM, Sánchez-López, S, Stoner, KE and Riba-Hernández, P (2009) Diet of spider monkeys (Ateles geoffroyi) in Mesoamerica: current knowledge and future directions. American Journal of Primatology: Official Journal of the American Society of Primatologists 71, 8–20. https://doi.org/10.1002/ajp.20625 CrossRefGoogle ScholarPubMed
Hargreaves, GH and Samani, ZA (1985) Reference crop evapotranspiration from temperature. Applied Engineering in Agriculture 1, 96–99. https://doi.org/10.13031/2013.26773 CrossRefGoogle Scholar
Hu, J and Riveros-Iregui, DA (2016) Life in the clouds: are tropical montane cloud forests responding to changes in climate? Oecologia 180, 1061–1073. https://doi.org/10.1007/s00442-015-3533-x CrossRefGoogle ScholarPubMed
Jarvis, A and Mulligan, M (2011) The climate of cloud forests. Hydrological Processes 25, 327–343. https://doi.org/10.1002/hyp.7847 CrossRefGoogle Scholar
Kovach Computing Services (2013) Oriana (version 4.02). Retrieved from https://www.kovcomp.co.uk/oriana/ Google Scholar
Lira-Torres, I, Naranjo-Piñera, EJ, Güiris-Andrade, DM and Cruz-Aldán, E (2004) Ecología de Tapirus bairdii (Perissodactyla: Tapiridae) en la Reserva de la Biosfera El Triunfo (Polígono 1), Chiapas, México. Acta Zoológica Mexicana 20, 1–21.CrossRefGoogle Scholar
Long, A and Heath, M (1991) Flora of the El Triunfo Biosphere Reserve, Chiapas, Mexico. A preliminary floristic inventory and the plant communities of Polygon 1. Anales del Instituto de Biología, Universidad Nacional Autónoma de México. Serie Botánica 62, 133–172.Google Scholar
Loope, LL and Giambelluca, TW (1998) Vulnerability of island tropical montane cloud forests to climate change, with special reference to East Maui, Hawaii. Climatic Change 39, 503–517. https://doi.org/10.1007/978-94-017-2730-3_18 CrossRefGoogle Scholar
Mendoza, I (2020) Estadística circular aplicada a la Ecología. Ecosistemas 29, 1995. https://doi.org/10.7818/ECOS.1995 Google Scholar
Mendoza, I, Peres, CA and Morellato, LPC (2017) Continental-scale patterns and climatic drivers of fruiting phenology: a quantitative Neotropical review. Global and Planetary Change 148, 227–241. https://doi.org/10.1016/j.gloplacha.2016.12.001 CrossRefGoogle Scholar
Montanaro, G, Dichio, B and Xiloyannis, C (2010) Significance of fruit transpiration on calcium nutrition in developing apricot fruit. Journal of Plant Nutrition and Soil Science 173, 618–622. https://doi.org/10.1002/jpln.200900376 CrossRefGoogle Scholar
Morellato, LPC, Alberti, LF and Hudson, IL (2010) Applications of circular statistics in plant phenology: a case studies approach. In Hudson, IL, Keatley, MR (eds), Phenological Research: Methods for Environmental and Climate Change Analysis (pp. 339–359). Dordrecht: Springer. https://doi.org/10.1007/978-90-481-3335-2_16 CrossRefGoogle Scholar
Murray-Tortarolo, G, Jaramillo, VJ, Maass, M, Friedlingstein, P and Sitch, S (2017) The decreasing range between dry-and wet-season precipitation over land and its effect on vegetation primary productivity. PLoS ONE 12, e0190304. https://doi.org/10.1371/journal.pone.0190304 CrossRefGoogle ScholarPubMed
Murray-Tortarolo, GN (2021) Seven decades of climate change across Mexico. Atmósfera 34, 217–226. https://doi.org/10.20937/atm.52803 Google Scholar
Numata, S, Yasuda, M, Okuda, T, Kachi, N and Noor, NSM (2003) Temporal and spatial patterns of mass flowerings on the Malay Peninsula. American Journal of Botany 90, 1025–1031. https://doi.org/10.3732/ajb.90.7.1025 CrossRefGoogle ScholarPubMed
Oshima, C, Tokumoto, Y and Nakagawa, M (2015) Biotic and abiotic drivers of dipterocarp seedling survival following mast fruiting in Malaysian Borneo. Journal of Tropical Ecology 31, 129–137. https://doi.org/10.1017/S026646741400073X CrossRefGoogle Scholar
Pau, S, Cordell, S, Ostertag, R, Inman, F and Sack, L (2020) Climatic sensitivity of species’ vegetative and reproductive phenology in a Hawaiian montane wet forest. Biotropica 52, 825–835. https://doi.org/10.1111/btp.12801 CrossRefGoogle Scholar
Pau, S, Wolkovich, EM, Cook, BI, Davies, TJ, Kraft, NJ, Bolmgren, K, Rodríguez Betancourt, JL and Cleland, EE (2011) Predicting phenology by integrating ecology, evolution and climate science. Global Change Biology 17, 3633–3643. https://doi.org/10.1111/j.1365-2486.2011.02515.x CrossRefGoogle Scholar
Quej, VH, Almorox, J, Ibrakhimov, M and Saito, L (2016) Empirical models for estimating daily global solar radiation in Yucatán Peninsula, Mexico. Energy Conversion and Management 110, 448–456. https://doi.org/10.1016/j.enconman.2015.12.050 CrossRefGoogle Scholar
R Core Team (2022) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/ Google Scholar
Ramírez, F and Davenport, TL (2016) The phenology of the capuli cherry [Prunus serotina subsp. capuli (Cav.) McVaugh] characterized by the BBCH scale, landmark stages and implications for urban forestry in Bogotá, Colombia. Urban Forestry & Urban Greening 19, 202–211. https://doi.org/10.1016/j.ufug.2016.06.028 CrossRefGoogle Scholar
Ramos-Robles, M, Andresen, E and Díaz-Castelazo, C (2016) Temporal changes in the structure of a plant-frugivore network are influenced by bird migration and fruit availability. PeerJ 4, e2048.CrossRefGoogle ScholarPubMed
Rojas-Soto, OR, Sosa, V and Ornelas, JF (2012) Forecasting cloud forest in eastern and southern Mexico: conservation insights under future climate change scenarios. Biodiversity and Conservation 21, 2671–2690. https://doi.org/10.1007/s10531-012-0327-x CrossRefGoogle Scholar
Solórzano, S (1995) Fenología de 22 especies arbóreas y su relación con la migración altitudinal del Quetzal (Pharomachrus mocinno mocinno De la Llave 1832) en la Reserva de la Biosfera El Triunfo. Chiapas, México (Bachelor thesis). Retrieved from Repositorio Institucional de la Universidad Nacional Autónoma de México.Google Scholar
Solórzano, S, Ávila, L, Castillo, S, Meave, JA and Ibarra-Manríquez, G (2010) Fenología de los árboles del bosque mesófilo de la Reserva de la Biosfera El Triunfo, Chiapas. In Pérez Farrera, MA, Tejeda Cruz, C, Silva Rivera, E (eds), Los bosques mesófilos de montaña en Chiapas: situación actual, diversidad y conservación (pp. 121–160). Tuxtla Gutiérrez, México: Universidad de Ciencias y Artes de Chiapas.Google Scholar
Solórzano, S, Castillo, S, Valverde, T and Ávila, L (2000) Quetzal abundance in relation to fruit availability in a cloud forest in southeastern Mexico. Biotropica 32, 523–532. https://doi.org/10.1111/j.1744-7429.2000.tb00498.x CrossRefGoogle Scholar
Tejeda-Cruz, C and Sutherland, WJ (2005) Cloud forest bird responses to unusually severe storm damage. Biotropica 37, 88–95. https://doi.org/10.1111/j.1744-7429.2005.03079.x CrossRefGoogle Scholar
Todeschini, F, Toledo, JJD, Rosalino, LM and Hilario, RR (2020) Niche differentiation mechanisms among canopy frugivores and zoochoric trees in the northeastern extreme of the Amazon. Acta Amazonica 50, 263–272. https://doi.org/10.1590/1809-4392202000732 CrossRefGoogle Scholar
Turc, L (1961) Estimation of irrigation water requirements, potential evapotranspiration: a simple climatic formula evolved up to date. Annales Agronomiques 12, 13–49.Google Scholar
Van Schaik, CP, Terborgh, JW and Wright, SJ (1993) The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annual Review of Ecology and Systematics 24, 353–377.CrossRefGoogle Scholar
Wheelwright, NT (1985) Competition for dispersers, and the timing of flowering and fruiting in a guild of tropical trees. Oikos 44, 465–477.CrossRefGoogle Scholar
Wheelwright, NT (1986) A seven-year study of individual variation in fruit production in tropical bird-dispersed tree species in the family Lauraceae. In Estrada, A, Flemming, TH (eds), Frugivores and Seed Dispersal (pp. 19–35). Dordrecht, Netherlands: Junk Publishers.CrossRefGoogle Scholar
Williams-Linera, G (1997) Phenology of deciduous and broadleaved-evergreen tree species in a Mexican tropical lower montane forest. Global Ecology and Biogeography Letters 6, 115–127.CrossRefGoogle Scholar
Williams-Linera, G, Alvarez-Aquino, C and Tolome, J (2021) Tree damage, growth and phenology after a hurricane in a tropical dry forest in Veracruz. Revista Mexicana de Ciencias Forestales 12, 185–201. https://doi.org/10.29298/rmcf.v12i67.858 CrossRefGoogle Scholar
Wootton, A (2022) Relaciones entre tendencias climáticas, patrones fenológicos y abundancia del quetzal en El Triunfo, Chiapas. (Unpublished doctoral thesis). El Colegio de la Frontera Sur, San Cristóbal de las Casas, Mexico.Google Scholar
Wootton, A, Enríquez, PL and Navarrete-Gutiérrez, D (2023) Regional patterns of vegetation, temperature, and rainfall trends in the coastal mountain range of Chiapas, Mexico. Atmósfera 36, 91–122. https://doi.org/10.20937/ATM.53026 Google Scholar
Wunderle, JM (1995) Responses of bird populations in a Puerto Rican forest to Hurricane Hugo: the first 18 months. The Condor 97, 879–896.CrossRefGoogle Scholar
Xu, K and Servedio, MR (2021) The evolution of flower longevity in unpredictable pollination environments. Journal of Evolutionary Biology 34, 1781–1792. https://doi.org/10.1111/jeb.13936 CrossRefGoogle ScholarPubMed
Zárate-Cuevas, L, Núñez-López, NM, Cuevas-Guzmán, R, Morales-Arias, JG, Sánchez-Rodríguez, EV, Guzmán-Hernández, L and Solís Magallanes, JA (2022) Fenología reproductiva de árboles en una zona montañosa del occidente de México. Revista Mexicana de Ciencias Forestales 13, 155–176. https://doi.org/10.29298/rmcf.v13i69.1176 CrossRefGoogle Scholar
Zimmerman, JK, Wright, SJ, Calderón, O, Pagan, MA and Paton, S (2007) Flowering and fruiting phenologies of seasonal and aseasonal neotropical forests: the role of annual changes in irradiance. Journal of Tropical Ecology 23, 231–251. https://doi.org/10.1017/S0266467406003890 CrossRefGoogle Scholar
Supplementary material: File

Wootton et al. supplementary material 1

Wootton et al. supplementary material
Download Wootton et al. supplementary material 1(File)
File 128.9 KB
Supplementary material: File

Wootton et al. supplementary material 2

Wootton et al. supplementary material
Download Wootton et al. supplementary material 2(File)
File 49.6 KB
Supplementary material: File

Wootton et al. supplementary material 3

Wootton et al. supplementary material
Download Wootton et al. supplementary material 3(File)
File 57.1 KB