Carbon pools recover more quickly than plant biodiversity in tropical secondary forests

Proceedings of the Royal Society B: Biological Sciences

Volumn 280, Issue 1773, 2013, Pages

  Martin, Philip A ^a,b   Newton, Adrian C ^b   Bullock, James M ^a  

^a CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

^b BOURNEMOUTH UNIVERSITY   (United Kingdom)

Author keywords

Biomass; Carbon; Forest restoration; Meta analysis; Plant biodiversity; Secondary forest

Indexed keywords

CARBON;

ABOVEGROUND BIOMASS; BIODIVERSITY; COLONIZATION; DISTURBANCE; EPIPHYTE; HABITAT RESTORATION; META-ANALYSIS; RESTORATION ECOLOGY; SECONDARY FOREST; SECONDARY SUCCESSION; SOIL CARBON; SPECIES RICHNESS; TROPICAL FOREST;

ARTICLE; BIODIVERSITY; BIOMASS; ENVIRONMENTAL PROTECTION; FOREST RESTORATION; META ANALYSIS; METABOLISM; PLANT BIODIVERSITY; PLANT PHYSIOLOGY; SECONDARY FOREST; TREE; TROPIC CLIMATE;

BIOMASS; CARBON; FOREST RESTORATION; META-ANALYSIS; PLANT BIODIVERSITY; SECONDARY FOREST;

BIODIVERSITY; CARBON; CONSERVATION OF NATURAL RESOURCES; METABOLISM; PLANT PHYSIOLOGICAL PHENOMENA; TREES; TROPICAL CLIMATE;

EID: 84894335791     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2013.2236     Document Type: Article

References (69)

1. Gardner TA, Barlow J, Sodhi NS, Peres CA. 2010 A multi-region assessment of tropical forest biodiversity in a human-modified world. Biol. Conserv. 143, 2293-2300. (doi:10.1016/j.biocon.2010.05.017)
2. Dixon RK, Solomon AM, Brown S, Houghton RA, Trexier MC, Wisniewski J. 1994 Carbon pools and flux of global forest ecosystems. Science 263, 185-190. (doi:10.1126/science.263.5144.185)
3. Gardner TA, Barlow J, Chazdon R, Ewers RM, Harvey CA, Peres CA, Sodhi NS. 2009 Prospects for tropical forest biodiversity in a human-modified world. Ecol. Lett. 12, 561-582. (doi:10.1111/j.1461-0248.2009.01294.x)
4. Foley JA et al. 2007 Amazonia revealed: forest degradation and loss of ecosystem goods and services in the Amazon Basin. Front. Ecol. Environ. 5, 25-32. (doi:10.1890/1540-9295(2007)5[25: ARFDAL]2.0.CO;2)
5. Gibbs HK, Ruesch AS, Achard F, Clayton MK, Holmgren P, Ramankutty N, Foley JA. 2010 Tropical forests were the primary sources of new agricultural land in the 1980s and 1990s. Proc. Natl Acad. Sci. USA 107, 16 732-16 737. (doi:10.1073/pnas. 0910275107)
6. Sayer J, Chokkalingam U, Poulsen J. 2004 The restoration of forest biodiversity and ecological values. Forest Ecol. Manag. 201, 3-11. (doi:10. 1016/j.foreco.2004.06.008)
7. Calmon M, Brancalion PHS, Paese A, Aronson J, Castro P, da Silva SC, Rodrigues RR. 2011 Emerging threats and opportunities for large-scale ecological restoration in the Atlantic forest of Brazil. Restor. Ecol. 19, 154-158. (doi:10.1111/j.1526-100X.2011.00772.x)
8. Alexander S et al. 2011 Opportunities and challenges for ecological restoration within REDD{thorn}. Restor. Ecol. 19, 683-689. (doi:10.1111/j.1526-100X.2011.00822.x)
9. CBD. 2010 Decision adopted by the Conference of the Parties to the Convention on Biological Diversity at its Tenth Meeting: the Strategic Plan for Biodiversity 2011-2020 and the Aichi Biodiversity Targets. See http://www.cbd.int/decisions/cop.
10. Silver WL, Ostertag R, Lugo AE. 2000 The potential for carbon sequestration through reforestation of abandoned tropical agricultural and pasture lands. Restor. Ecol. 8, 394-407. (doi:10.1046/j.1526-100x.2000.80054.x)
11. Mari{dotless}́n-Spiotta E, Sharma S. 2012 Carbon storage in successional and plantation forest soils: a tropical analysis. Glob. Ecol. Biogeogr. 22, 105-117. (doi:10.1111/j.1466-8238.2012.00788.x)
12. Anderson KJ, Allen AP, Gillooly JF, Brown JH. 2006 Temperature-dependence of biomass accumulation rates during secondary succession. Ecol. Lett. 9, 673-682. (doi:10.1111/j.1461-0248.2006.00914.x)
13. Johnson CM, Zarin DJ, Johnson AH. 2000 Postdisturbance aboveground biomass accumulation in global secondary forests. Ecology 81, 1395-1401. (doi:10.1890/0012-9658(2000)081[1395:pdabai]2.0. co;2)
14. Brown S, Lugo AE. 1990 Tropical secondary forests. J. Trop. Ecol. 6, 1-32. (doi:10.1017/S026646740000 3989)
15. Hughes RF, Kauffman JB, Jaramillo VJ. 1999 Biomass, carbon, and nutrient dynamics of secondary forests in a humid tropical region of México. Ecology 80, 1892-1907. (doi:10.2307/ 176667)
16. Saldarriaga JG, West DC, Tharp M, Uhl C. 1988 Long-term chronosequence of forest succession in the upper Rio Negro of Colombia and Venezuela. J. Ecol. 76, 938-958. (doi:10.2307/2260625)
17. Cifuentes-Jara M. 2008 Aboveground biomass and ecosystem carbon pools in tropical secondary forests growing in six life zones of Costa Rica. Ann Arbor, MI: ProQuest.
18. Read L, Lawrence D. 2003 Recovery of biomass following shifting cultivation in dry tropical forests of the Yucatan. Ecol. Appl. 13, 85-97. (doi:10. 1890/1051-0761(2003)013[0085:ROBFSC]2.0.CO;2)
19. Guo LB, Gifford RM. 2002 Soil carbon stocks and land use change: a meta analysis. Glob. Change Biol. 8, 345-360. (doi:10.1046/j.1354-1013.2002.00486.x)
20. Rhoades CC, Eckert GE, Coleman DC. 2000 Soil carbon differences among forest, agriculture, and secondary vegetation in Lower Montane Ecuador. Ecol. Appl. 10, 497-505. (doi:10.1890/1051-0761(2000)010[0497:SCDAFA]2.0.CO;2)
21. 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. Forest Ecol. Manag. 261, 1625-1633. (doi:10.1016/j.foreco.2010.07.023)
22. Saynes V, Hidalgo C, Etchevers JD, Campo JE. 2005 Soil C and N dynamics in primary and secondary seasonally dry tropical forests in Mexico. Appl. Soil Ecol. 29, 282-289. (doi:10.1016/j.apsoil.2004.11.007)
23. Dunn RR. 2004 Recovery of faunal communities during tropical forest regeneration. Conserv. Biol. 18, 302-309. (doi:10.1111/j.1523-1739.2004.00151.x)
24. Dent DH, Wright SJ. 2009 The future of tropical species in secondary forests: a quantitative review. Biol. Conserv. 142, 2833-2843. (doi:10.1016/j. biocon.2009.05.035)
25. Chazdon RL, Peres CA, Dent D, Sheil D, Lugo AE, Lamb D, Stork NE, Miller SE. 2009 The potential for species conservation in tropical secondary forests. Conserv. Biol. 23, 1406-1417. (doi:10.1111/j.1523-1739.2009.01338.x)
26. Corlett RT. 1994 What is secondary forest? J. Trop. Ecol. 10, 445-447. (doi:10.1017/S026646740000 8129)
27. Newbold T, Scharlemann JPW, Butchart SHM, Şekercioǧlu ÇH, Alkemade R, Booth H, Purves DW. 2013 Ecological traits affect the response of tropical forest bird species to land-use intensity. Proc. R. Soc. B 280, 20122131. (doi:10.1098/rspb.2012.2131)
28. Pullin AS, Stewart GB. 2006 Guidelines for systematic review in conservation and environmental management. Conserv. Biol. 20, 1647-1656. (doi:10. 1111/j.1523-1739.2006.00485.x)
29. Gibson L et al. 2011 Primary forests are irreplaceable for sustaining tropical biodiversity. Nature 478, 378-381. (doi:10.1038/nature10425)
30. Holdridge LR. 1967 Life zone ecology. San Jose, CA: Tropical Science Center.
31. Johnson EA, Miyanishi K. 2008 Testing the assumptions of chronosequences in succession. Ecol. Lett. 11, 419-431. (doi:10.1111/j.1461-0248.2008.01173.x)
32. Baker TR et al. 2004 Increasing biomass in Amazonian forest plots. Phil. Trans. R. Soc. Lond. B 359, 353-365. (doi:10.1098/rstb.2003.1422)
33. Rey Benayas JM, Newton AC, Diaz A, Bullock JM. 2009 Enhancement of biodiversity and ecosystem services by ecological restoration: a meta-analysis. Science 325, 1121-1124. (doi:10.1126/science. 1172460)
34. Moreno-Mateos D, Power ME, Comi{dotless}́n FA, Yockteng R. 2012 Structural and functional loss in restored wetland ecosystems. PLoS Biol. 10, e1001247. (doi:10.1371/journal.pbio.1001247)
35. Putz FE et al. 2012 Sustaining conservation values in selectively logged tropical forests: the attained and the attainable. Conserv. Lett. 5, 296-303. (doi:10.1111/j.1755-263X.2012.00242.x)
36. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS. 2009 Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol. Evol. 24, 127-135. (doi:10.1016/j.tree.2008.10.008)
37. Chave J et al. 2005 Tree allometry and improved estimation of carbon stocks and balance in tropical forests. Oecologia 145, 87-99. (doi:10.1007/ s00442-005-0100-x)
38. Barlow J et al. 2007 Quantifying the biodiversity value of tropical primary, secondary, and plantation forests. Proc. Natl Acad. Sci. USA 104, 18 555-18 560. (doi:10.1073/pnas.0703333104)
39. Chazdon RL et al. 2011 A novel statistical method for classifying habitat generalists and specialists. Ecology 92, 1332-1343. (doi:10.1890/10-1345.1)
40. Burnham KP, Anderson DR, Huyvaert KP. 2011 AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav. Ecol. Sociobiol. 65, 23-35. (doi:10.1007/s00265-010-1029-6)
41. Nakagawa S, Schielzeth H. 2013 A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4, 133-142. (doi:10.1111/j.2041-210x.2012.00261.x)
42. R Development Core Team. 2011 R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
43. Barton K. 2013 MuMIn: multi-model inference (1.9.5 ed). See http://cran.r-project.org/web/ packages/MuMIn/index.html.
44. Wickham H. 2009 ggplot2: elegant graphics for data analysis. New York, NY: Springer.
45. Saatchi SS et al. 2011 Benchmark map of forest carbon stocks in tropical regions across three continents. Proc. Natl Acad. Sci. USA 108, 9899-9904. (doi:10.1073/pnas.1019576108)
46. Guariguata MR, Ostertag R. 2001 Neotropical secondary forest succession: changes in structural and functional characteristics. Forest Ecol. Manag. 148, 185-206. (doi:10.1016/S0378-1127(00) 00535-1)
47. Lindenmayer DB et al. In press. New policies for old trees: averting a global crisis in a keystone ecological structure. Conserv. Lett. (doi:10.1111/ conl.12013)
48. 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. Forest Ecol. Manag. 262, 1648-1657. (doi:10.1016/j.foreco.2011.07.018)
49. Montgomery RA, Chazdon RL. 2001 Forest structure, canopy architecture, and light transmittance in tropical wet forests. Ecology 82, 2707-2718. (doi:10.2307/2679955)
50. Cairns MA, Brown S, Helmer EH, Baumgardner GA. 1997 Root biomass allocation in the world's upland forests. Oecologia 111, 1-11. (doi:10.1007/ s004420050201)
51. Fearnside PM, Guimarães WM. 1996 Carbon uptake by secondary forests in Brazilian Amazonia. Forest Ecol. Manag. 80, 35-46. (doi:10.1016/0378-1127(95) 03648-2)
52. Mokany K, Raison R, Prokushkin AS. 2006 Critical analysis of root: shoot ratios in terrestrial biomes. Glob. Change Biol. 12, 84-96. (doi:10.1111/j.1365-2486.2005.001043.x)
53. Don A, Schumacher J, Freibauer A. 2011 Impact of tropical land-use change on soil organic carbon stocks: a meta-analysis. Glob. Change Biol. 17, 1658-1670. (doi:10.1111/j.1365-2486.2010.02336.x).
54. Marin-Spiotta E, Silver WL, Swanston CW, Ostertag R. 2009 Soil organic matter dynamics during 80 years of reforestation of tropical pastures. Glob. Change Biol. 15, 1584-1597. (doi:10.1111/j.1365-2486.2008.01805.x)
55. Chazdon RL, Letcher SG, van Breugel M, Marti{dotless}́nez-Ramos M, Bongers F, Finegan B. 2007 Rates of change in tree communities of secondary Neotropical forests following major disturbances. Phil. Trans. R. Soc. B 362, 273-289. (doi:10.1098/rstb.2006.1990)
56. Eaton JM, Lawrence D. 2009 Loss of carbon sequestration potential after several decades of shifting cultivation in the Southern Yucatán. Forest Ecol. Manag. 258, 949-958. (doi:10.1016/j.foreco.2008.10.019)
57. Lawrence D. 2005 Biomass accumulation after 10-200 years of shifting cultivation in Bornean rain forest. Ecology 86, 26-33. (doi:10.1890/03-0564)
58. KöSter N, Friedrich K, Nieder J, Barthlott W. 2009 Conservation of epiphyte diversity in an andean landscape transformed by human land use Conservación de la Diversidad de Epi{dotless}́fitas en una Paisaje Andino Transformado por Uso de Suelo Humano. Conserv. Biol. 23, 911-919. (doi:10.1111/ j.1523-1739.2008.01164.x)
59. Woods CL, DeWalt SJ. 2013 The conservation value of secondary forests for vascular epiphytes in Central Panama. Biotropica 45, 119-127. (doi:10.1111/j. 1744-7429.2012.00883.x)
60. Benitez-Malvido J. 1998 Impact of forest fragmentation on seedling abundance in a tropical rain forest. Conserv. Biol. 12, 380-389. (doi:10.1111/j.1523-1739.1998.96295.x)
61. Turner IM, Corlett TR. 1996 The conservation value of small, isolated fragments of lowland tropical rain forest. Trends Ecol. Evol. 11, 330-333. (doi:10. 1016/0169-5347(96)10046-X)
62. Condit R et al. 2002 Beta-diversity in tropical forest trees. Science 295, 666-669. (doi:10.1126/science. 1066854)
63. Ramage BS et al. 2012 Pseudoreplication in tropical forests and the resulting effects on biodiversity conservation. Conserv. Biol. 27, 364-372. (doi:10. 1111/cobi.12004)
64. Ebeling J, Yasué M. 2008 Generating carbon finance through avoided deforestation and its potential to create climatic, conservation and human development benefits. Phil. Trans. R. Soc. B 363, 1917-1924. (doi:10.1098/rstb.2007.0029)
65. Venter O, Meijaard E, Possingham H, Dennis R, Sheil D, Wich S, Hovani L, Wilson K. 2009 Carbon payments as a safeguard for threatened tropical mammals. Conserv. Lett. 2, 123-129. (doi:10.1111/ j.1755-263X.2009.00059.x)
66. Bekessy SA, Wintle BA. 2008 Using carbon investment to grow the biodiversity bank. Conserv. Biol. 22, 510-513. (doi:10.1111/j.1523-1739.2008.00943.x)
67. 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. (doi:10.1111/j.1744-7429.2006.00228.x)
68. IUCN SSC. 2001 IUCN Red List categories and criteria: v 3.1. Prepared by the IUCN Species Survival Commission. See http://www.iucnredlist.org/ technical-documents/categories-and-criteria/2001-categories-criteria.
69. Benayas JMR, Bullock JM, Newton AC. 2008 Creating woodland islets to reconcile ecological restoration, conservation, and agricultural land use. Front. Ecol. Environ. 6, 329-336. (doi:10.1890/070057)