Secondary forest fragments offer important carbon and biodiversity cobenefits

Global Change Biology

Volumn 26, Issue 2, 2020, Pages 509-522

  Matos, Fabio A R ^a,b,c,d   Magnago, Luiz F S ^e   Aquila Chan Miranda, Carlos ^b   de Menezes, Luis F T ^d   Gastauer, Markus ^f   Safar, Nathália V H ^a   Schaefer, Carlos E G R ^a   da Silva, Mônica P ^g   Simonelli, Marcelo ^h   Edwards, Felicity A ⁱ   Martins, Sebastião V ^a   Meira Neto, João A A ^a   Edwards, David P ^b  

^a FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c Departamento de Biologia Geral   (Brazil)

^d FEDERAL UNIVERSITY OF ESPÍRITO SANTO   (Brazil)

^e Instituto de Estudos Socioambientais   (Brazil)

^f INSTITUTO TECNOLÓGICO VALE   (Brazil)

^g Ciencia e Tecnologia Baiano   (Brazil)

^h INSTITUTO FEDERAL DO ESPÍRITO SANTO   (Brazil)

ⁱ LANCASTER UNIVERSITY   (United Kingdom)

Author keywords

biomass; Brazilian Atlantic Forest; ecosystems services; endemic species richness; Forest and Landscape Restoration; REDD+; threatened

Indexed keywords

BIODIVERSITY; BIOMASS; CARBON; DEFORESTATION; ECOSYSTEM SERVICE; EMISSION CONTROL; ENDEMIC SPECIES; FRAGMENTATION; RESTORATION ECOLOGY; TROPICAL FOREST;

ATLANTIC FOREST; BRAZIL;

BOS;

ANIMAL; BIODIVERSITY; BOVINE; BRAZIL; ECOSYSTEM; ENVIRONMENTAL PROTECTION; FOREST; PHYLOGENY; TROPIC CLIMATE;

ANIMALS; BIODIVERSITY; BRAZIL; CATTLE; CONSERVATION OF NATURAL RESOURCES; ECOSYSTEM; FORESTS; PHYLOGENY; TROPICAL CLIMATE;

EID: 85074790131     PISSN: 13541013     EISSN: 13652486     Source Type: Journal    
DOI: 10.1111/gcb.14824     Document Type: Article

References (67)

1. Banks-Leite, C., Pardini, R., Tambosi, L. R., Pearse, W. D., Bueno, A. A., Bruscagin, R. T., … Metzger, J. P. (2014). Using ecological thresholds to evaluate the costs and benefits of set-asides in a biodiversity hotspot. Science, 345(6200), 1041–1045. https://doi.org/10.1126/science.1255768
2. Barlow, J., Gardner, T. A., Araujo, I. S., Avila-Pires, T. C., Bonaldo, A. B., Costa, J. E., … Peres, C. A. (2007). Quantifying the biodiversity value of tropical primary, secondary, and plantation forests. Proceedings of the National Academy of Sciences of the United States of America, 104(47), 18555–18560. https://doi.org/10.1073/pnas.0703333104
3. Barnett, J., Adger, W. N. J. P. G. (2007). Climate change, human security and violent conflict. Political Geography, 26(6), 639–655. https://doi.org/10.1016/j.polgeo.2007.03.003
4. Barton, K. (2019). Package ‘MuMIn’. Model selection and model averaging base on information criteria. R package version 1.43.6. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from https://cran.r-project.org/web/packages/MuMIn/index.html
5. Basham, E., González del Pliego, P., Acosta-Galvis, A., Woodcock, P., Medina Uribe, C., Haugaasen, T., … Edwards, D. J. A. C. (2016). Quantifying carbon and amphibian co-benefits from secondary forest regeneration in the Tropical Andes. Animal Conservation, 19(6), 548–560. https://doi.org/10.1111/acv.12276
6. Bello, C., Galetti, M., Pizo, M. A., Magnago, L. F. S., Rocha, M. F., Lima, R. A. F., … Jordano, P. (2015). Defaunation affects carbon storage in tropical forests. Science Advances, 1(11), e1501105. https://doi.org/10.1126/sciadv.1501105
7. Bivand, R., & Piras, G. (2015). Comparing implementations of estimation methods for spatial econometrics. Journal of Statistical Software, 63(18), 1–35. https://doi.org/10.18637/jss.v063.i18
8. Burnham, K. P., Anderson, D. R. (2002). Model selection and multimodel inference: A practical information-theoretic approach (2nd ed., pp. 1–488). New York, NY: Springer.
9. Burnham, K. P., Anderson, D. R., & Huyvaert, K. P. (2011). AIC model selection and multimodel inference in behavioral ecology: Some background, observations, and comparisons. Behavioral Ecology and Sociobiology, 65(1), 23–35. https://doi.org/10.1007/s00265-010-1084-z
10. Busch, J., Engelmann, J., Cook-Patton, S. C., Griscom, B. W., Kroeger, T., Possingham, H., & Shyamsundar, P. (2019). Potential for low-cost carbon dioxide removal through tropical reforestation. Nature Climate Change, 9(6), 463–466. https://doi.org/10.1038/s41558-019-0485-x
11. Cardinale, B. J., Duffy, J. E., Gonzalez, A., Hooper, D. U., Perrings, C., Venail, P., … Naeem, S. (2012). Biodiversity loss and its impact on humanity. Nature, 486, 59. https://doi.org/10.1038/nature11148
12. Chao, A., Chazdon, R. L., Colwell, R. K., & Shen, T.-J. (2005). A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecology Letters, 8(2), 148–159. https://doi.org/10.1111/j.1461-0248.2004.00707.x
13. Chase, M. W., Christenhusz, M. J. M., Fay, M. F., Byng, J. W., Judd, W. S., … Stevens, P. F. (2016). An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society, 181(1), 1–20. https://doi.org/10.1111/boj.12385
14. Chave, J., Coomes, D., Jansen, S., Lewis, S. L., Swenson, N. G., & Zanne, A. E. (2009). Towards a worldwide wood economics spectrum. Ecology Letters, 12(4), 351–366. https://doi.org/10.1111/j.1461-0248.2009.01285.x
15. Chave, J., Réjou-Méchain, M., Búrquez, A., Chidumayo, E., Colgan, M. S., Delitti, W. B. C., … Vieilledent, G. (2014). Improved allometric models to estimate the aboveground biomass of tropical trees. Global Change Biology, 20(10), 3177–3190. https://doi.org/10.1111/gcb.12629
16. Colwell, R. K. (2013). EstimateS: Statistical estimation of species richness and shared species from samples. Version 9.1.0. User's Guide and application. Retrieved from http://purl.oclc.org/estimates
17. Corlett, R. (1994). What is secondary forest? Journal of Tropical Ecology, 10(3), 445–447. https://doi.org/10.1017/S0266467400008129
18. Edwards, D. P., Massam, M. R., Haugaasen, T., & Gilroy, J. J. (2017). Tropical secondary forest regeneration conserves high levels of avian phylogenetic diversity. Biological Conservation, 209, 432–439. https://doi.org/10.1016/j.biocon.2017.03.006
19. Faith, D. P. (1992). Conservation evaluation and phylogenetic diversity. Biological Conservation, 61(1), 1–10. https://doi.org/10.1016/0006-3207(92)91201-3
20. Ferraz, G., Russell, G. J., Stouffer, P. C., Bierregaard, R. O., Pimm, S. L., & Lovejoy, T. E. (2003). Rates of species loss from Amazonian forest fragments. Proceedings of the National Academy of Sciences of the United States of America, 100(24), 14069–14073. https://doi.org/10.1073/pnas.2336195100
21. Ferreira, J., Lennox, G. D., Gardner, T. A., Thomson, J. R., Berenguer, E., Lees, A. C., … Barlow, J. (2018). Carbon-focused conservation may fail to protect the most biodiverse tropical forests. Nature Climate Change, 8(8), 744–749. https://doi.org/10.1038/s41558-018-0225-7
22. Field, C. B., Behrenfeld, M. J., Randerson, J. T., & Falkowski, P. (1998). Primary production of the biosphere: Integrating terrestrial and oceanic components. Science, 281(5374), 237–240. https://doi.org/10.1126/science.281.5374.237
23. Flores, O., & Coomes, D. A. (2011). Estimating the wood density of species for carbon stock assessments. Methods in Ecology and Evolution, 2(2), 214–220. https://doi.org/10.1111/j.2041-210X.2010.00068.x
24. Frishkoff, L. O., Karp, D. S., M'Gonigle, L. K., Mendenhall, C. D., Zook, J., Kremen, C., … Daily, G. C. (2014). Loss of avian phylogenetic diversity in neotropical agricultural systems. Science, 345(6202), 1343–1346. https://doi.org/10.1126/science.1254610
25. Gastauer, M., Caldeira, C. F., Trotter, I., Ramos, S. J., & Meira Neto, J. A. A. (2018). Optimizing community trees using the open tree of life increases the reliability of phylogenetic diversity and dispersion indices. Ecological Informatics, 46, 192–198. https://doi.org/10.1016/j.ecoinf.2018.06.008
26. Gellie, N. J., Breed, M. F., Mortimer, P. E., Harrison, R. D., Xu, J., & Lowe, A. J. (2018). Networked and embedded scientific experiments will improve restoration outcomes. Frontiers in Ecology and the Environment, 16(5), 288–294. https://doi.org/10.1002/fee.1810
27. Gibbs, H. K., Ruesch, A. S., Achard, F., Clayton, M. K., Holmgren, P., Ramankutty, N., & Foley, J. A. (2010). Tropical forests were the primary sources of new agricultural land in the 1980s and 1990s. Proceedings of the National Academy of Sciences of the United States of America, 107(38), 16732–16737. https://doi.org/10.1073/pnas.0910275107
28. Gibson, L., Lee, T. M., Koh, L. P., Brook, B. W., Gardner, T. A., Barlow, J., … Sodhi, N. S. (2011). Primary forests are irreplaceable for sustaining tropical biodiversity. Nature, 478, 378. https://doi.org/10.1038/nature10425
29. Gilroy, J. J., Woodcock, P., Edwards, F. A., Wheeler, C., Baptiste, B. L. G., Medina Uribe, C. A., … Edwards, D. P. (2014). Cheap carbon and biodiversity co-benefits from forest regeneration in a hotspot of endemism. Nature Climate Change, 4, 503. https://doi.org/10.1038/nclimate2200
30. Gouvêa, J. B. S. (1969). Contribuição à geomorfologia do sul da Bahia. Área dos baixos cursos dos rios Pardo e Jequitinhonha. Comunicação Técnica do Cenntro De Pesquisas do CACAU/Comissão Executiva De Planejamento Da Lavoura Cacaueira, Itabuna, 35, 1–111.
31. Haddad, N. M., Brudvig, L. A., Clobert, J., Davies, K. F., Gonzalez, A., Holt, R. D., … Townshend, J. R. (2015). Habitat fragmentation and its lasting impact on earth's ecosystems. Science Advances, 1(2), e1500052. https://doi.org/10.1126/sciadv.1500052
32. Hammer, Ø., Harper, D. A., Ryan, P. D. J. P. E. (2001). PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4(1), 9.
33. Hansen, M. C., Potapov, P. V., Moore, R., Hancher, M., Turubanova, S. A., Tyukavina, A., … Townshend, J. R. G. (2013). High-resolution global maps of 21st-century forest cover change. Science, 342(6160), 850–853. https://doi.org/10.1126/science.1244693
34. Hothorn, T. F., Bretz, P., Westfall, R. M., Heiberger, A., Schuetzenmeister, A., & Scheibe, S. (2017). Package ‘multcomp’: simultaneous models. Version 1.4-8. Retrieved from https://cran.csiro.au/web/packages/multcomp/index.html
35. Hubbell, S. P. (2001). The unified neutral theory of biodiversity and biogeography (MPB-32). Princeton, NJ: Princeton University Press.
36. IBGE (Fundação Instituto Brasileiro de Geografia e Estatística). (1987). Rio Doce: geologia, geomorfologia, pedologia, vegetação e uso potencial da terra. Projeto Radambrasil, Volume SF.34, Rio de Janeiro.
37. Laliberté, E., Wells, J. A., DeClerck, F., Metcalfe, D. J., Catterall, C. P., Queiroz, C., … Mayfield, M. M. (2010). Land-use intensification reduces functional redundancy and response diversity in plant communities. Ecology Letters, 13(1), 76–86. https://doi.org/10.1111/j.1461-0248.2009.01403.x
38. Laurance, W. F., Lovejoy, T. E., Vasconcelos, H. L., Bruna, E. M., Didham, R. K., Stouffer, P. C., … Sampaio, E. (2002). Ecosystem decay of Amazonian forest fragments: A 22-year investigation. Conservation Biology, 16(3), 605–618. https://doi.org/10.1046/j.1523-1739.2002.01025.x
39. Lennox, G. D., Gardner, T. A., Thomson, J. R., Ferreira, J., Berenguer, E., Lees, A. C., … Barlow, J. (2018). Second rate or a second chance? Assessing biomass and biodiversity recovery in regenerating Amazonian forests. Global Change Biology, 24(12), 5680–5694. https://doi.org/10.1111/gcb.14443
40. Lewis, S. L., Edwards, D. P., & Galbraith, D. (2015). Increasing human dominance of tropical forests. Science, 349(6250), 827–832. https://doi.org/10.1126/science.aaa9932
41. Lohbeck, M., Bongers, F., Martinez-Ramos, M., & Poorter, L. (2016). The importance of biodiversity and dominance for multiple ecosystem functions in a human-modified tropical landscape. Ecology, 97(10), 2772–2779. https://doi.org/10.1002/ecy.1499
42. Lohbeck, M., Poorter, L., Paz, H., Pla, L., van Breugel, M., Martínez-Ramos, M., & Bongers, F. (2012). Functional diversity changes during tropical forest succession. Perspectives in Plant Ecology, Evolution and Systematics, 14(2), 89–96. https://doi.org/10.1016/j.ppees.2011.10.002
43. Magallón, S., Gómez-Acevedo, S., Sánchez-Reyes, L. L., & Hernández-Hernández, T. (2015). A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity. New Phytologist, 207(2), 437–453. https://doi.org/10.1111/nph.13264
44. Magnago, L. F. S., Edwards, D. P., Edwards, F. A., Magrach, A., Martins, S. V., & Laurance, W. F. (2014). Functional attributes change but functional richness is unchanged after fragmentation of Brazilian Atlantic forests. Journal of Ecology, 102(2), 475–485. https://doi.org/10.1111/1365-2745.12206
45. Magnago, L. F. S., Magrach, A., Laurance, W. F., Martins, S. V., Meira-Neto, J. A. A., Simonelli, M., & Edwards, D. P. (2015). Would protecting tropical forest fragments provide carbon and biodiversity cobenefits under REDD+? Global Change Biology, 21(9), 3455–3468. https://doi.org/10.1111/gcb.12937
46. Malhi, Y., Baker, T. R., Phillips, O. L., Almeida, S., Alvarez, E., Arroyo, L., … Lloyd, J. (2004). The above-ground coarse wood productivity of 104 neotropical forest plots. Global Change Biology, 10(5), 563–591. https://doi.org/10.1111/j.1529-8817.2003.00778.x
47. Matos, F. A. R., Magnago, L. F. S., Gastauer, M., Carreiras, J. M. B., Simonelli, M., Meira-Neto, J. A. A., & Edwards, D. P. (2017). Effects of landscape configuration and composition on phylogenetic diversity of trees in a highly fragmented tropical forest. Journal of Ecology, 105(1), 265–276. https://doi.org/10.1111/1365-2745.12661
48. McCarthy, D. P., Donald, P. F., Scharlemann, J. P. W., Buchanan, G. M., Balmford, A., Green, J. M. H., … Butchart, S. H. M. (2012). Financial costs of meeting global biodiversity conservation targets: Current spending and unmet needs. Science, 338(6109), 946–949. https://doi.org/10.1126/science.1229803
49. Pavoine, S., & Bonsall, M. B. (2011). Measuring biodiversity to explain community assembly: A unified approach. Biological Reviews, 86(4), 792–812. https://doi.org/10.1111/j.1469-185X.2010.00171.x
50. Pavoine, S., Vallet, J., Dufour, A.-B., Gachet, S., & Daniel, H. (2009). On the challenge of treating various types of variables: Application for improving the measurement of functional diversity. Oikos, 118(3), 391–402. https://doi.org/10.1111/j.1600-0706.2008.16668.x
51. Peixoto, A. L., & Gentry, A. (1990). Diversidade e composição florísitica da mata de tabuleiro na Reserva Florestal de Linhares (Espírito Santo, Brasil). Revista Brasileira De Botânica, 13, 19–25.
52. Petchey, O. L., & Gaston, K. J. (2002). Functional diversity (FD), species richness and community composition. Ecology Letters, 5(3), 402–411. https://doi.org/10.1046/j.1461-0248.2002.00339.x
53. Phelps, J., Webb, E. L., & Adams, W. M. (2012). Biodiversity co-benefits of policies to reduce forest-carbon emissions. Nature Climate Change, 2, 497. https://doi.org/10.1038/nclimate1462
54. Pimm, S. L., Jenkins, C. N., Abell, R., Brooks, T. M., Gittleman, J. L., Joppa, L. N., … Sexton, J. O. (2014). The biodiversity of species and their rates of extinction, distribution, and protection. Science, 344(6187), 1246752. https://doi.org/10.1126/science.1246752
55. Poorter, L., Bongers, F., Aide, T. M., Almeyda Zambrano, A. M., Balvanera, P., Becknell, J. M., … Rozendaal, D. M. A. (2016). Biomass resilience of Neotropical secondary forests. Nature, 530, 211. https://doi.org/10.1038/nature16512
56. QGIS Development Team. (2017). QGIS Geographic Information System. 2.18.5-Dufour Open Source Geospatial Foundation Project. Retrieved from https://qgis.org/en/site/about/index.html
57. R Development Core Team. (2018). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
58. Réjou-Méchain, M., Tanguy, A., Piponiot, C., Chave, J., & Hérault, B. (2017). biomass: An r package for estimating above-ground biomass and its uncertainty in tropical forests. Methods in Ecology and Evolution, 8(9), 1163–1167. https://doi.org/10.1111/2041-210x.12753
59. Ribeiro, M. C., Metzger, J. P., Martensen, A. C., Ponzoni, F. J., & Hirota, M. M. (2009). The Brazilian Atlantic forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation, 142(6), 1141–1153. https://doi.org/10.1016/j.biocon.2009.02.021
60. Rolim, S. G., Jesus, R. M., Nascimento, H. E. M., do Couto, H. T. Z., & Chambers, J. Q. (2005). Biomass change in an Atlantic tropical moist forest: The ENSO effect in permanent sample plots over a 22-year period. Oecologia, 142(2), 238–246. https://doi.org/10.1007/s00442-004-1717-x
61. Senior, R. A., Hill, J. K., González Del Pliego, P., Goode, L. K., & Edwards, D. P. (2017). A pantropical analysis of the impacts of forest degradation and conversion on local temperature. Ecology and Evolution, 7(19), 7897–7908. https://doi.org/10.1002/ece3.3262
62. The IUCN. (2018). Red List of Threatened Species. Version 2018.2. Retrieved from https://www.iucnredlist.org/
63. Turner, W. R., Oppenheimer, M., & Wilcove, D. S. (2009). A force to fight global warming. Nature, 462, 278. https://doi.org/10.1038/462278a
64. 2 emissions from forest loss. Nature Geoscience, 2, 737. https://doi.org/10.1038/ngeo671
65. Veron, S., Davies, T. J., Cadotte, M. W., Clergeau, P., & Pavoine, S. (2015). Predicting loss of evolutionary history: Where are we? Biological Review, 92(1), 271–291. https://doi.org/10.1111/brv.12228
66. Webb, C. O. (2000). Exploring the phylogenetic structure of ecological communities: An example for rain forest trees. The American Naturalist, 156(2), 145–155. https://doi.org/10.1086/303378
67. Webb, C. O., Ackerly, D. D., & Kembel, S. W. (2008). Phylocom: Software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics, 24(18), 2098–2100. https://doi.org/10.1093/bioinformatics/btn358