Succession of ephemeral secondary forests and their limited role for the conservation of floristic diversity in a human-modified tropical landscape

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Van Breugel, Michiel ^a   Hall, Jefferson S ^a   Craven, Dylan ^a,b,d   Bailon, Mario ^a   Hernandez, Andres ^a   Abbene, Michele ^b   Van Breugel, Paulo ^c  

^a SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

^b Yale School of the Environment   (United States)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d GERMAN CENTRE FOR INTEGRATIVE BIODIVERSITY RESEARCH IDIV HALLE JENA LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT TREE; ARTICLE; EPHEMERAL SECONDARY FOREST SUCCESSION; EPHEMERAL SPECIES; FOREST DYNAMICS; JUVENILE PLANT; LANDSCAPE ECOLOGY; NONHUMAN; PANAMA; PLANT DISPERSAL; PLANT LIFE CYCLE STAGE; PLANT REPRODUCTION; POPULATION ABUNDANCE; SECONDARY SUCCESSION (COMMUNITY); SOIL QUALITY; SPECIES COMPOSITION; SPECIES CONSERVATION; SPECIES DIVERSITY; TROPICAL RAIN FOREST;

BIODIVERSITY; CONSERVATION OF NATURAL RESOURCES; ECOSYSTEM; HUMANS; PANAMA; TREES; TROPICAL CLIMATE;

EID: 84892409811     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082433     Document Type: Article

References (95)

1. International Tropical Timber Organization (2002) ITTO guidelines for the restoration, management and rehabilitation of degraded and secondary tropical forests. Yokohama, Japan: International Tropical Timber Organization. 84 p. Available: http://www.itto.int/policypapers-guidelines/. Accessed 15 January 2013.
2. Food and Agricultural Organization (2011) State of the World's Forests. Rome: Food and Agriculture Organization of the United Nations. 164 p. Available: http://www.fao.org/docrep/013/i2000e/i2000e00.htm. Accessed 20 January 2013.
3. Asner GP, Rudel TK, Aide TM, Defries R, Emerson R (2009) A contemporary assessment of change in humid tropical forests. Conserv Biol 23: 1386-1395.
4. Chazdon Robin RL, Peres CA, Dent DH, Sheil D, Lugo AE, et al. (2009) The Potential for Species Conservation in Tropical Secondary Forests. Conserv Biol 23: 1406-1417.
5. Harvey CA, Komar O, Chazdon R, Ferguson BG, Finegan B, et al. (2008) Integrating agricultural landscapes with biodiversity conservation in the Mesoamerican hotspot. Conserv Biol 22: 8-15.
6. Wright SJ, Muller-Landau HC (2006) The Future of Tropical Forest Species1. Biotropica 38: 287-301.
7. Grau HR, Aide TM (2008) Globalization and Land-Use Transitions in Latin America. Ecol Soc 13: 16.
8. Lugo AE, Helmer E (2004) Emerging forests on abandoned land: Puerto Rico's new forests. For Ecol Manage 190: 145-161.
9. Finegan B, Nasi R (2004) The biodiversity and conservation potential of shifting cultivation landscapes. In: Schroth G, da Fonseca GAB, Harvey CA, Gason C, Vasconcelos HL, et al., editors. Agroforestry and biodiversity conservation in tropical landscapes. Washington DC: Island Press. pp. 153-197.
10. Moran EF, Packer A, Brondizio E, Tucker J (1996) Restoration of vegetation cover in the eastern Amazon. Ecol Econ 18: 41-54.
11. Neeff T, Lucas RM, dos Santos JR, Brondizio ES, Freitas CC (2006) Area and Age of Secondary Forests in Brazilian Amazonia 1978-2002: An Empirical Estimate. Ecosystems 9: 609-623.
12. Perz SG, Aramburú C, Bremner J (2005) Population, Land Use and Deforestation in the Pan Amazon Basin: a Comparison of Brazil, Bolivia, Colombia, Ecuador, Perú and Venezuela. Environ Dev Sustain 7: 23-49.
13. Metzger J (2002) Landscape dynamics and equilibrium in areas of slash-and-burn agriculture with short and long fallow period (Bragantina region, NE Brazilian Amazon). Landsc Ecol 17: 419-431.
14. Gardner TA, Barlow J, Parry LW, Peres CA (2007) Predicting the Uncertain Future of Tropical Forest Species in a Data Vacuum. Biotropica 39: 25-30.
15. Melo FPL, Arroyo-Rodríguez V, Fahrig L, Martínez-Ramos M, Tabarelli M (2013) On the hope for biodiversity-friendly tropical landscapes. Trends Ecol Evol: 1-7.
16. Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, et al. (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7: 601-613.
17. Grubb PJ (1977) The maintenance of species richness in plant communities: The importance of the regeneration niche. Biol Rev 52: 107-145.
18. Bazzaz FA (1996) Plants in changing environments: linking physiological, population, and community ecology. Cambridge: Cambridge University Press. 320 p.
19. Grime JP (2002) Plant strategies, vegetation processes, and ecosystem properties. West SussexUK: John Wiley & Sons Inc. 417 p.
20. Chazdon R, Carson W (2008) Chance and determinism in tropical forest succession. In: Carson WP, Schnitzer SA, editors. Tropical forest community. West Sussex, UK: Wiley-Blackwell. pp. 384-408.
21. Rees M, Condit R, Crawley M, Pacala S, Tilman D (2001) Long-term studies of vegetation dynamics. Science 293: 650-655.
22. Calcagno V, Mouquet N, Jarne P, David P (2006) Coexistence in a metacommunity: the competition-colonization trade-off is not dead. Ecol Lett 9: 897-907.
23. Muller-Landau HC (2010) The tolerance-fecundity trade-off and the maintenance of diversity in seed size. Proc Natl Acad Sci 107: 4242-4247.
24. Brook BW, Bradshaw CJA, Koh LP, Sodhi NS (2006) Momentum Drives the Crash: Mass Extinction in the Tropics1. Biotropica 38: 302-305.
25. Gibson L, Lee TM, Koh LP, Brook BW, Gardner TA, et al. (2011) Primary forests are irreplaceable for sustaining tropical biodiversity. Nature 478: 378-381.
26. Laurance WF (2007) Have we overstated the tropical biodiversity crisis? Trends Ecol Evol 22: 65-70.
27. Bossuyt B, Honnay O (2006) Interactions between plant life span, seed dispersal capacity and fecundity determine metapopulation viability in a dynamic landscape. Landsc Ecol 21: 1195-1205.
28. Ogden FL, Crouch TD, Stallard R., Hall JS (2013) Effect of Land Cover and Use on Dry Season River Discharge and Peak Flows in the Seasonal Tropics of Central Panama. Water Recourses Res: in review.
29. Turner BL, Engelbrecht BMJ (2010) Soil organic phosphorus in lowland tropical rain forests. Biogeochemistry 103: 297-315.
30. Neumann-Cosel L, Zimmermann B, Hall JS, van Breugel M, Elsenbeer H (2011) Soil carbon dynamics under young tropical secondary forests on former pastures - A case study from Panama. For Ecol Manage 261: 1625-1633.
31. Hassler SK, Zimmermann B, van Breugel M, Hall JS, Elsenbeer H (2011) Recovery of saturated hydraulic conductivity under secondary succession on former pasture in the humid tropics. For Ecol Manage 261: 1634-1642.
32. Croat TB (1978) Flora of Barro Colorado Island. Stanford, California, U.S.A.: Stanford University Press. 943 p.
33. Leigh EG (1999) Tropical Forest Ecology. A View from Barro Colorado Island. OxfordUK: Oxford University Press. 264 p.
34. van Breugel M, Ransijn J, Craven D, Bongers F, Hall JS (2011) Estimating carbon stock in secondary forests: Decisions and uncertainties associated with allometric biomass models. For Ecol Manage 262: 1648-1657.
35. Gerwing JJ, Schnitzer SA, Burnham RJ, Bongers F, Chave J, et al. (2006) A Standard Protocol for Liana Censuses. Biotropica 38: 256-261.
36. Schnitzer SA, DeWalt SJ, Chave J (2006) Censusing and Measuring Lianas: A Quantitative Comparison of the Common Methods. Biotropica 38: 581-591.
37. Chazdon RL, Letcher SG, van Breugel M, Martínez-Ramos M, Bongers F, et al. (2007) Rates of change in tree communities of secondary Neotropical forests following major disturbances. Philos Trans R Soc Lond B Biol Sci 362: 273-289.
38. Johnson EA, Miyanishi K (2008) Testing the assumptions of chronosequences in succession. Ecol Lett 11: 419-431.
39. Foster BL, Tilman D (2000) Dynamic and static views of succession: testing the descriptive power of the chronosequence approach. Plant Ecol 146: 1-10.
40. Walker LR, Wardle DA, Bardgett RD, Clarkson BD (2010) The use of chronosequences in studies of ecological succession and soil development. J Ecol 98: 725-736.
41. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, et al. (2013) vegan: Community Ecology Package.
42. Oksanen J (2013) Multivariate Analysis of Ecological Communities in R: vegan tutorial. Available: http://vegan.r-forge.r-project.org/.
43. Magurran AE (2004) Measuring biological diversity. MaldenMA, USA: Blackwell Publishing. 260 p.
44. Hill MO (1973) Diversity and Evenness: A Unifying Notation and Its Consequences. Ecology 54: 427.
45. Jost L (2006) Entropy and diversity. Oikos 113: 363-375.
46. Chao A, Chiu C-H, Hsieh TC (2012) Proposing a resolution to debates on diversity partitioning. Ecology 93: 2037-2051.
47. Whittaker RH (1972) Evolution and Measurement of Species Diversity. Taxon 21: 213.
48. Jost L (2010) The Relation between Evenness and Diversity. Diversity 2: 207-232.
49. Venables WN, Ripley BD (2002) Modern applied statistics with S. 4th ed. New York: Springer. 495 p.
50. Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4: 379-391.
51. van Breugel M, Martínez-Ramos M, Bongers F (2006) Community dynamics during early secondary succession in Mexican tropical rain forests. J Trop Ecol 22: 663-674.
52. Lebrija-Trejos E, Pérez-García EA, Meave JA, Bongers F, Poorter L (2010) Functional traits and environmental filtering drive community assembly in a species-rich tropical system. Ecology 91: 386-398.
53. Anderson MJ, Crist TO, Chase JM, Vellend M, Inouye BD, et al. (2011) Navigating the multiple meanings of b diversity: a roadmap for the practicing ecologist. Ecol Lett 14: 19-28.
54. McCune B, Grace JB, Urban DL (2002) Analysis of ecological communities. Gleneden Beach OR: MjM Software Design Gleneden Beach, OR.
55. Chao A, Chazdon RL, Colwell RK, Shen TJ (2005) A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecol Lett 8: 148-159.
56. Chao A, Chazdon RL, Colwell RK, Shen T-J (2006) Abundance-based similarity indices and their estimation when there are unseen species in samples. Biometrics 62: 361-371.
57. Wolda H (1981) Similarity indices, sample size and diversity. Oecologia 50: 296-302.
58. Condit R, Engelbrecht BMJ, Pino D, Pérez R, Turner BL (2013) Species distributions in response to individual soil nutrients and seasonal drought across a community of tropical trees. Proc Natl Acad Sci U S A.
59. Wright SJ, Jaramillo MA, Pavon J, Condit R, Hubbell SP, et al. (2005) Reproductive size thresholds in tropical trees: variation among individuals, species and forests. J Trop Ecol 21: 307-315.
60. Norden N, Chazdon RL, Chao A, Jiang Y-H, Vílchez-Alvarado B (2009) Resilience of tropical rain forests: tree community reassembly in secondary forests. Ecol Lett 12: 385-394.
61. Jayakumar S, Kim SS, Heo J (2011) Floristic inventory and diversity assessment - a critical review. Proceedings of the International Academy of Ecology and Environmental Sciences 1: 151-168.
62. López-Martínez JO, Sanaphre-Villanueva L, Dupuy JM, Hernández-Stefanoni JL, Meave JA, et al. (2013) b-Diversity of functional groups of woody plants in a tropical dry forest in Yucatan. PLoS One 8: e73660.
63. Ruiz J, Fandino MC, Chazdon RL (2005) Vegetation Structure, Composition, and Species Richness Across a 56-year Chronosequence of Dry Tropical Forest on Providencia Island, Colombia1. Biotropica 37: 520-530.
64. Van Breugel M, Bongers F, Martínez-Ramos M (2007) Species Dynamics During Early Secondary Forest Succession: Recruitment, Mortality and Species Turnover. Biotropica 39: 610-619.
65. Norden N, Chazdon RL, Chao A, Jiang Y-H, Vílchez-Alvarado B (2009) Resilience of tropical rain forests: tree community reassembly in secondary forests. Ecol Lett 12: 385-394.
66. Dent DH, DeWalt SJ, Denslow JS (2013) Secondary forests of central Panama increase in similarity to old-growth forest over time in shade tolerance but not species composition. J Veg Sci 24: 530-542.
67. van Breugel M, van Breugel P, Jansen PA, Martínez-Ramos M, Bongers F (2011) The relative importance of above- versus belowground competition for tree growth during early succession of a tropical moist forest. Plant Ecol 213: 25-34.
68. Neumann-Cosel L, Zimmermann B, Hall JS, van Breugel M, Elsenbeer H (2010) Soil carbon dynamics under young tropical secondary forests on former pastures - A case study from Panama. For Ecol Manage.
69. Hurtt GC, Pacala SW (1995) The consequences of recruitment limitation: reconciling chance, history and competitive differences between plants. J Theor Biol 176: 1-12.
70. Mayfield MM, Ackerly D, Daily GC (2006) The diversity and conservation of plant reproductive and dispersal functional traits in human-dominated tropical landscapes. J Ecol 94: 522-536.
71. Cramer JM, Mesquita RCG, Bruce Williamson G (2007) Forest fragmentation differentially affects seed dispersal of large and small-seeded tropical trees. Biol Conserv 137: 415-423.
72. Lopes de Melo FP, Dirzo R, Tabarelli M (2006) Biased seed rain in forest edges: Evidence from the Brazilian Atlantic forest. Biol Conserv 132: 50-60.
73. Wunderle JM (1997) The role of animal seed dispersal in accelerating native forest regeneration on degraded tropical lands. For Ecol Manage 99: 223-235.
74. Holl KD (1999) Factors limiting tropical rain forest regeneration in abandoned pasture: seed rain, seed germination, microclimate, and soil. Biotropica 31: 229-242.
75. Chazdon RL, Chao A, Colwell RK, Lin S-Y, Norden N, et al. (2011) A novel statistical method for classifying habitat generalists and specialists. Ecology 92: 1332-1343.
76. Gomez-Pompa A, Vazquez-Yanes C (1981) Successional studies of a rain forest in Mexico. In: West DC, Shugart HH, Botkin DB, editors. Forest concepts and application. New York: Springer-Verlag. pp. 247-266.
77. Finegan B (1996) Pattern and process in neotropical secondary rain forests: the first 100 years of succession. Trends Ecol Evol 11: 119-124.
78. Hillebrand H, Bennett DM, Cadotte MW (2008) Consequences of dominance: a review of evenness effects on local and regional ecosystem processes. Ecology 89: 1510-1520.
79. Holl KD, Aide TM (2011) When and where to actively restore ecosystems? For Ecol Manage 261: 1558-1563.
80. Thomas SC (1996) Reproductive allometry in Malaysian rain forest trees: Biomechanics versus optimal allocation. Evol Ecol 10: 517-530.
81. Alvarez-Buylla ER, Martinez-Ramos M (1992) Demography and allometry of Cecropia obtusifolia, a neotropical pioneer tree-an evaluation of the climax-pioneer paradigm for tropical rain forests. J Ecol 80: 275-290.
82. Barlow J, Gardner TA, Louzada J, Peres CA (2010) Measuring the conservation value of tropical primary forests: the effect of occasional species on estimates of biodiversity uniqueness. PLoS One 5: e9609.
83. Dias PC (1996) Sources and sinks in population biology. Trends Ecol Evol 11: 326-330.
84. 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 Manage 256: 1910-1917.
85. Harrison RD, Tan S, Plotkin JB, Slik F, Detto M, et al. (2013) Consequences of defaunation for a tropical tree community. Ecol Lett.
86. Santos BA, Peres CA, Oliveira M a., Grillo A, Alves-Costa CP, et al. (2008) Drastic erosion in functional attributes of tree assemblages in Atlantic forest fragments of northeastern Brazil. Biol Conserv 141: 249-260.
87. Lawrence D (2004) Erosion of tree diversity during 200 years of shifting cultivation in Bornean rain forest. Ecol Appl 14: 1855-1869.
88. Cardoso da Silva JM, Tabarelli M (2000) Tree species impoverishment and the future flora of the Atlantic forest of northeast Brazil. Nature 404: 72-74.
89. Laurance WF, Nascimento HEM, Laurance SG, Andrade A, Ewers RM, et al. (2007) Habitat fragmentation, variable edge effects, and the landscape-divergence hypothesis. PLoS One 2: e1017.
90. Etter A, McAlpine C, Pullar D, Possingham H (2005) Modeling the age of tropical moist forest fragments in heavily-cleared lowland landscapes of Colombia. For Ecol Manage 208: 249-260.
91. Tilman D, May RM, Lehman CL, Nowak MA (1994) Habitat destruction and the extinction debt. Nature 371: 65-66.
92. Dullinger S, Essl F, Rabitsch W, Erb K-H, Gingrich S, et al. (2013) Europe's other debt crisis caused by the long legacy of future extinctions. Proc Natl Acad Sci.
93. Vellend M, Verheyen K, Jacquemyn H, Kolb A, Van Calster H, et al. (2006) Extinction debt of forest plants persists for more than a century following habitat fragmentation. Ecology 87: 542-548.
94. Tabarelli M, Aguiar AV, Ribeiro MC, Metzger JP, Peres CA (2010) Prospects for biodiversity conservation in the Atlantic Forest: Lessons from aging human-modified landscapes. Biol Conserv 143: 2328-2340.
95. Mehlich A (1984) Mehlich 3 soil test extractant: A modification of Mehlich 2 extractant. Commun Soil Sci Plant Anal 15: 1409-1416.