Abstract
Humans are transforming the ecology of the Earth through rapid changes in land use and climate. These changes can affect tropical forest structure, dynamics and diversity. While numerous studies have focused on diversity metrics, other aspects of forest function, such as long-term biomass dynamics, are often less considered. We evaluated plant community structure change (i.e., abundance, diversity, composition, and aboveground biomass) in a 2.25 ha forest dynamics plot located within a ~ 365 ha reserve in southern Costa Rica. We censused, mapped and identified to species all plants ≥ 5 cm diameter at breast height (DBH) in three surveys spanning 2010–2020. While there were no changes in late-successional species diversity, there were marked changes in overall species composition and biomass. Abundance of large (≥ 40 cm DBH) old-growth dense-wooded trees (e.g., Lauraceae, Rosaceae) decreased dramatically (27%), leading to major biomass decline over time, possibly driven by recent and recurrent drought events. Gaps created by large trees were colonized by early-successional species, but these recruits did not make up for the biomass lost. Finally, stem abundance increased by 20%, driven by increasing dominance of Hampea appendiculata. While results suggest this reserve may effectively conserve overall plant diversity, this may mask other key shifts such as large aboveground biomass loss. If this pattern is pervasive across tropical forest reserves, it could hamper efforts to preserve forest structure and ecosystem services (e.g., carbon storage). Monitoring programs could better assess carbon trends in reserves over time simply by tracking large tree dynamics.
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References
Aleixo I, Norris D, Hemerik L, Barbosa A, Prata E, Costa F et al (2019) Amazonian rainforest tree mortality driven by climate and functional traits. Nat Clim Chang 9:384–388. https://doi.org/10.1038/s41558-019-0458-0
Arroyo-Rodríguez V, Saldaña-Vázquez RA, Fahrig L, Santos BA (2017) Does forest fragmentation cause an increase in forest temperature? Ecol Res 32:81–88. https://doi.org/10.1007/s11284-016-1411-6
Avolio ML, Carroll IT, Collins SL, Houseman GR, Hallett LM, Isbell F et al (2019) A comprehensive approach to analyzing community dynamics using rank abundance curves. Ecosphere. https://doi.org/10.1002/ecs2.2881
Bennett AC, McDowell NG, Allen CD, Anderson-Teixeira KJ (2015) Larger trees suffer most during drought in forests worldwide. Nat Plants 1:1–5. https://doi.org/10.1038/nplants.2015.139
Bongers F, Ewango CEN, van der Sande MT, Poorter L (2020) Liana species decline in Congo basin contrasts with global patterns. Ecology 101:e03004. https://doi.org/10.1002/ecy.3004
Chave J, Andalo C, Brown S, Cairns MA, Chambers JQ, Eamus D et al (2005) Tree allometry and improved estimation of carbon stocks and balance in tropical forests. Oecologia 145:87–99. https://doi.org/10.1007/s00442-005-0100-x
Chave J, Muller-Landau HC, Baker TR, Easdale TA, ter Steege H, Webb CO (2006) Regional and phylogenetic variation of wood density across 2456 neotropical tree species. Ecol Appl 16:2356–2367. https://doi.org/10.1890/1051-0761(2006)016[2356:RAPVOW]2.0.CO;2
Chazdon RL, Chao A, Colwell RK, Lin SY, Norden N, Letcher SG et al (2011) A novel statistical method for classifying habitat generalists and specialists. Ecology 92:1332–1343
Clark DA, Piper SC, Keeling CD, Clark DB (2003) Tropical rain forest tree growth and atmospheric carbon dynamics linked to interannual temperature variation during 1984–2000. Proc Natl Acad Sci 100:5852–5857. https://doi.org/10.1073/pnas.0935903100
Condit R (1998) Tropical forest census plots: methods and results from barro Colorado Island, panama and a comparison with other plots. Springer-Verlag, Heidelberg
Condit R, Pérez R, Lao S, Aguilar S, Hubbell SP (2017) Demographic trends and climate over 35 years in the Barro Colorado 50 ha plot. For Ecosyst 4:17. https://doi.org/10.1186/s40663-017-0103-1
Crutzen PJ (2002) Geology of mankind. Nature 415:23–23. https://doi.org/10.1038/415023a
de Souza RP, Válio IFM (2001) Seed size, seed germination, and seedling survival of Brazilian tropical tree species differing in successional status1. Biotropica 33:447–457. https://doi.org/10.1111/j.1744-7429.2001.tb00198.x
Dietze MC, Matthes JH (2014) A general ecophysiological framework for modelling the impact of pests and pathogens on forest ecosystems. Ecol Lett 17:1418–1426. https://doi.org/10.1111/ele.12345
Ellis EC (2015) Ecology in an anthropogenic biosphere. Ecol Monogr 85:287–331. https://doi.org/10.1890/14-2274.1
Ellis EC (2019) Evolution: biodiversity in the Anthropocene. Curr Biol 29:R831–R833. https://doi.org/10.1016/j.cub.2019.07.073
Espírito-Santo FDB, Gloor M, Keller M, Malhi Y, Saatchi S, Nelson B et al (2014) Size and frequency of natural forest disturbances and the Amazon forest carbon balance. Nat Commun 5:3434. https://doi.org/10.1038/ncomms4434
Esquivel-Muelbert A, Baker TR, Dexter KG, Lewis SL, Brienen RJW, Feldpausch TR et al (2019) Compositional response of Amazon forests to climate change. Glob Change Biol 25:39–56. https://doi.org/10.1111/gcb.14413
Fontes CG, Chambers JQ, Higuchi N (2018) Revealing the causes and temporal distribution of tree mortality in Central Amazonia. For Ecol Manag 424:177–183. https://doi.org/10.1016/j.foreco.2018.05.002
FRA (2020) Global forest resources assessment 2020. FAO
Haber W (2000) Plants and vegetation. In: Nadkarni NM, Wheelwright NT (eds) Monteverde: ecology and conservation of a tropical cloud forest. Oxford University Press, New York
Hansen MC, Potapov PV, Moore R, Hancher M, Turubanova SA, Tyukavina A et al (2013) High-resolution global maps of 21st-century forest cover change. Science 342:850–853. https://doi.org/10.1126/science.1244693
Jin VL, West LT, Haines BL, Peterson CJ (2000) P retention in tropical pre-montane soils across forest-pastures interfaces. Soil Sci 165:881–889
Jost L (2006) Entropy and diversity. Oikos 113:363–375. https://doi.org/10.1111/j.2006.0030-1299.14714.x
Laurance WF (2002) Hyperdynamism in fragmented habitats. J Veg Sci 13:595–602. https://doi.org/10.1111/j.1654-1103.2002.tb02086.x
Laurance WF, Laurance SG, Ferreira LV, Merona JMR, Gascon C, Lovejoy TE (1997) Biomass collapse in Amazonian forest fragments. Science 278:1117–1118. https://doi.org/10.1126/science.278.5340.1117
Laurance WF, Camargo JLC, Luizão RCC, Laurance SG, Pimm SL, Bruna EM et al (2011) The fate of Amazonian forest fragments: a 32 year investigation. Biol Conserv 144:56–67. https://doi.org/10.1016/j.biocon.2010.09.021
Laurance WF, Useche DC, Rendeiro J, Kalka M, Bradshaw CJA, Sloan SP (2012) Averting biodiversity collapse in tropical forest protected areas. Nature 489:290–294. https://doi.org/10.1038/nature11318
LCBS (2016) A partial listing of the trees registered in the Las Cruces area. In: Las Cruces Res. Stn.-Organ. Trop. Stud. https://tropicalstudies.org/portfolio/las-cruces-research-station/. Accessed 21 Aug 2020
Leitold V, Morton DC, Longo M, dos Santos MN, Keller M, Scaranello M (2018) El Niño drought increased canopy turnover in Amazon forests. New Phytol 219:959–971. https://doi.org/10.1111/nph.15110
Malhi Y, Franklin J, Seddon N, Solan M, Turner MG, Field CB et al (2020) Climate change and ecosystems: threats, opportunities and solutions. Philos Trans R Soc B Biol Sci 375:20190104. https://doi.org/10.1098/rstb.2019.0104
Marcon E, Herault B (2015) entropart: an R package to measure and partition diversity. J Stat Softw 67:1–26. https://doi.org/10.18637/jss.v067.i08
Martínez-Ramos M, Ortiz-Rodríguez IA, Piñero D, Dirzo R, Sarukhán J (2016) Anthropogenic disturbances jeopardize biodiversity conservation within tropical rainforest reserves. Proc Natl Acad Sci USA 113:5323–5328. https://doi.org/10.1073/pnas.1602893113
Matelson TJ, Nadkarni NM, Solano R (1995) Tree damage and annual mortality in a montane forest in Monteverde, Costa Rica. Biotropica 27:441–447. https://doi.org/10.2307/2388956
Nepstad D, Tohver I, Ray D, Moutinho P, Cardinot G (2007) Mortality of large trees and lianas following experimental drought in an Amazon forest. Ecology. https://doi.org/10.1890/06-1046.1
Newbold T, Hudson LN, Contu S, Hill SLL, Beck J, Liu Y et al (2018) Widespread winners and narrow-ranged losers: land use homogenizes biodiversity in local assemblages worldwide. PLOS Biol 16:e2006841. https://doi.org/10.1371/journal.pbio.2006841
NOAA NWS (2021) Climate Prediction Center. https://origin.cpc.ncep.noaa.gov/products/analysis_monitoring/ensostuff/ONI_v5.php. Accessed 14 Apr 2021
Oliveira MA, Santos AMM, Tabarelli M (2008) Profound impoverishment of the large-tree stand in a hyper-fragmented landscape of the Atlantic forest. For Ecol Manag 256:1910–1917. https://doi.org/10.1016/j.foreco.2008.07.014
Paula MD, Costa CPA, Tabarelli M (2011) Carbon storage in a fragmented landscape of Atlantic Forest: the role played by edge-affected habitats and emergent trees. Trop Conserv Sci 4:349–358. https://doi.org/10.1177/194008291100400310
Phillips OL, Gentry AH (1994) Increasing turnover through time in tropical forests. Science 263:954–958. https://doi.org/10.1126/science.263.5149.954
Phillips OL, Baker TR, Arroyo L, Higuchi N, Killeen TJ, Laurance WF et al (2004) Pattern and process in Amazon tree turnover, 1976–2001. Philos Trans R Soc Lond B Biol Sci. https://doi.org/10.1098/rstb.2003.1438
QGIS Development Team (2016) QGIS Geographic Information System. Version 2.18. Open Source Geospatial Foundation. URL http://qgis.org
R Development Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing
Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153. https://doi.org/10.1016/j.biocon.2009.02.021
Rich PV, Rich TH (1983) The Central American dispersal route: biotic history and paleogeography. Costa Rican natural history, Janzen D.H. The University of Chicago Press, Chicago, pp 12–34
Rowland L, da Costa ACL, Galbraith DR, Oliveira RS, Binks OJ, Oliveira AAR et al (2015) Death from drought in tropical forests is triggered by hydraulics not carbon starvation. Nature 528:119–122. https://doi.org/10.1038/nature15539
Rowland L, da Costa ACL, Oliveira AAR, Bittencourt PL, Costa PB, Giles AL et al (2018) Drought stress and tree size determine stem CO2 efflux in a tropical forest. New Phytol 218:1393–1405
Schnitzer SA, Bongers F (2002) The ecology of lianas and their role in forests. Trends Ecol Evol 17:223–230. https://doi.org/10.1016/S0169-5347(02)02491-6
Schnitzer SA, DeWalt SJ, Chave J (2006) Censusing and measuring lianas: a quantitative comparison of the common methods. Biotropica 38:581–591. https://doi.org/10.1111/j.1744-7429.2006.00187.x
Snow DW (1981) Tropical frugivorous birds and their food plants: a world survey. Biotropica 13:1–14. https://doi.org/10.2307/2387865
Sullivan MJP, Lewis SL, Affum-Baffoe K, Castilho C, Costa F, Sanchez AC et al (2020) Long-term thermal sensitivity of Earth’s tropical forests. Science 368:869–874. https://doi.org/10.1126/science.aaw7578
Tabarelli M, Lopes AV, Peres CA (2008) Edge-effects drive tropical forest fragments towards an early-successional system. Biotropica 40:657–661. https://doi.org/10.1111/j.1744-7429.2008.00454.x
Tabarelli M, Peres CA, Melo FPL (2012) The ‘few winners and many losers’ paradigm revisited: emerging prospects for tropical forest biodiversity. Biol Conserv 155:136–140. https://doi.org/10.1016/j.biocon.2012.06.020
Thom D, Seidl R (2016) Natural disturbance impacts on ecosystem services and biodiversity in temperate and boreal forests: disturbance impacts on biodiversity and services. Biol Rev. https://doi.org/10.1111/brv.12193
Urquiza-Haas T, Dolman PM, Peres CA (2007) Regional scale variation in forest structure and biomass in the Yucatan Peninsula, Mexico: effects of forest disturbance. For Ecol Manag 247:80–90. https://doi.org/10.1016/j.foreco.2007.04.015
Vicente-Serrano SM, Beguería S, López-Moreno JI (2010) A multi-scalar drought index sensitive to global warming: the standardized precipitation evapotranspiration index–SPEI. J Clim 23:1696–1718. https://doi.org/10.1175/2009JCLI2909.1
Vilanova E, Ramírez-Angulo H, Torres-Lezama A, Aymard G, Gámez L, Durán C et al (2018) Environmental drivers of forest structure and stem turnover across Venezuelan tropical forests. PLoS ONE 13:e0198489. https://doi.org/10.1371/journal.pone.0198489
Zahawi RA, Duran G, Kormann U (2015) Sixty-seven years of land-use change in Southern Costa Rica. PLoS ONE 10:e0143554. https://doi.org/10.1371/journal.pone.0143554
Zahawi RA, Oviedo-Brenes F, Peterson CJ (2017) A degradation debt? Large-scale shifts in community composition and loss of biomass in a tropical forest fragment after 40 years of isolation. PLoS ONE 12:e0183133. https://doi.org/10.1371/journal.pone.0183133
Acknowledgements
We thank the Las Cruces Biological Station (Organization for Tropical Studies) for logistical support and access to the forest dynamics plot. We thank Juan Abel Rosales, Chris Graham, Javier Fernández, Víctor Meza, and many volunteers for their assistance in establishing the plot and conducting surveys.
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RAZ, FOB, and CJP contributed to the study conception and design. All authors performed data collection. FOB made taxonomic identification. MSJ and LW made data analyses. The first draft of the manuscript was written by MSJ and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Communicated by Marie-Josée Fortin.
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San-José, M., Werden, L., Peterson, C.J. et al. Large tree mortality leads to major aboveground biomass decline in a tropical forest reserve. Oecologia 197, 795–806 (2021). https://doi.org/10.1007/s00442-021-05048-w
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DOI: https://doi.org/10.1007/s00442-021-05048-w