bioRxiv preprint doi: https://doi.org/10.1101/2020.09.08.287938; this version posted September 9, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 The erosion of biodiversity and biomass in the Atlantic Forest 2 biodiversity hotspot 3 Renato A. F. Lima1,2*, Alexandre A. Oliveira1, Gregory R. Pitta1, André L. de Gasper3, 4 Alexander C. Vibrans4, Jérôme Chave5, Hans ter Steege2,6 & Paulo I. Prado1 5 6 1 Departamento de Ecologia, Instituto de Biociências, Universidade de São Paulo. Rua do 7 Matão, trav. 14, 321, 05508-090, São Paulo, Brazil. 8 2 Naturalis Biodiversity Center, Darwinweg 2, 2333 CR Leiden, The Netherlands. 9 3 Departamento de Ciências Naturais, Universidade Regional de Blumenau. Rua Antônio 10 da Veiga, 140, 89030-903, Blumenau, Brazil. 11 4 Departamento de Engenharia Florestal, Universidade Regional de Blumenau. Rua São 12 Paulo, 3250, 89030-000, Blumenau, Brazil. 13 5 Laboratoire Evolution et Diversité Biologique, UMR 5174 CNRS, Université Paul 14 Sabatier, IRD. 118, route de Narbonne, 31062, Toulouse, France. 15 6 Systems Ecology, Vrije Universiteit, De Boelelaan 1087, Amsterdam, 1081 HV, 16 Netherlands 17 *e-mail: [email protected] 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.09.08.287938; this version posted September 9, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 18 Abstract 19 Tropical forests are being deforested worldwide, and the remaining fragments are 20 suffering from biomass and biodiversity erosion. Quantifying this erosion is challenging 21 because ground data on tropical biodiversity and biomass are often sparse. Here, we use 22 an unprecedented dataset of 1,819 field surveys covering the entire Atlantic Forest 23 biodiversity hotspot. We show that 83−85% of the surveys presented losses in forest 24 biomass and tree species richness, functional traits and conservation value. On average, 25 forest fragments had 25−32% less biomass, 23−31% fewer species, and 33%, 36% and 26 42% fewer individuals of late-successional, large-seeded and endemic species, 27 respectively. Biodiversity and biomass erosion were both lower inside strictly protected 28 conservation units, particularly in large ones. We estimate that biomass erosion across the 29 Atlantic Forest remnants was equivalent to the loss of 55−70 thousand km2 of forests or 30 US$2.3−2.6 billion in carbon credits. These figures have direct implications on 31 mechanisms of climate change mitigation. 32 33 Introduction 34 Tropical forests are major stocks of biodiversity and carbon; and these stocks are 35 declining worldwide. Half of their original cover has already vanished and current 36 deforestation rates are about 1% per year1. Human impacts on tropical forests, however, 37 are not restricted to deforestation. Beyond the reduction in habitat availability and 38 connectivity, deforestation triggers a myriad of modifications that can penetrate up to 1.5 39 km into the remaining fragments2–4. In addition, forest fragments are more accessible, 40 increasing their exposure to fire, selective logging, hunting, and biological invasions. bioRxiv preprint doi: https://doi.org/10.1101/2020.09.08.287938; this version posted September 9, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 41 These human-induced impacts on forest fragments (i.e. forest degradation) impose a 42 long-lasting burden on forest biodiversity and biomass stocks5–12 that can be as severe as 43 deforestation13,14. Protected areas can mitigate the erosion of biodiversity and biomass15– 44 17, but their effectiveness is contingent on the type of management and level of 45 anthropogenic pressure surrounding the protected areas15–17. 46 Forest degradation can be assessed by high-resolution remote sensing (e.g. 47 LiDAR18), but the coverage of this approach is limited and the impact on biodiversity 48 cannot be measured. This is why large-scale quantifications of the impacts of forest 49 degradation are mostly available for biomass10–12. Therefore, field surveys remain 50 essential to quantify the erosion of both biodiversity and biomass2–4,7,8,10,19. The 51 simultaneous evaluation of forest degradation on tropical biodiversity and biomass at 52 large-scales provides crucial knowledge for the conservation and climate change 53 agenda13,17,20 and to refine regional assessments of biodiversity and ecosystem service 54 (e.g. Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services 55 - IPBES). 56 Here, we aim at quantifying the impacts of forest degradation on a major 57 biodiversity hotspot located in eastern South America, the Atlantic Forest 58 (Supplementary Fig. 1). Home to 35% of the South American population, the Atlantic 59 Forest is one of the most fragmented tropical/subtropical forests in the world12,21, which 60 may well represent the present or future of other tropical forests worldwide22. To achieve 61 our goal, we create one of the largest data sets of forest surveys ever assembled for the 62 tropics and subtropics23, both inside and outside protected areas. This data set includes 63 data on forest biomass and tree species richness and/or composition, as well as carefully bioRxiv preprint doi: https://doi.org/10.1101/2020.09.08.287938; this version posted September 9, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 64 curated metadata associated with each survey, representing a total of 1,819 field surveys, 65 1.45 million trees, 3,124 tree species, and 1,238 ha of sampling coverage (Supplementary 66 Table 1, Supplementary Data 1). The data set covers the entire range of environmental 67 conditions, landscape contexts, and disturbance histories of the Atlantic Forest 68 (Supplementary Fig. 2, Supplementary Table 2). It also contains information on multiple 69 species properties, including plant functional traits (i.e., wood density, maximum height, 70 seed mass), ecological groups (or successional status, e.g. pioneer) and their conservation 71 value (i.e., threat status and endemism level), which enable to assess human-induced 72 impacts on community composition sensu lato. 73 Using this unprecedented data set, we quantified forest degradation impacts on the 74 aboveground biomass stocks, tree species richness, and multiple species properties. More 75 specifically, we assess the extent and magnitude of those impacts by asking: (i) how 76 pervasive negative impacts are across this biodiversity hotspot? (ii) how much these 77 biodiversity and biomass losses represent compared to low-disturbance Atlantic Forests? 78 And (iii) can protected areas mitigate those losses? Next, we explore the implications of 79 our results to the conservation of what's left of this biodiversity hotspot by (iv) projecting 80 forest degradation impacts to the remaining Atlantic Forest area to estimate the total 81 amount of carbon lost. We also (v) explore the costs and benefit of two contrasting 82 restoration scenarios: one that focused only on reducing the within-fragment disturbance 83 level (i.e. ‘fragment restoration’ scenario) and another focused on increasing fragment 84 size and landscape connectivity (i.e. ‘landscape restoration’ scenario). 85 In general lines, we quantified forest degradation impacts on Atlantic Forest 86 biodiversity and biomass as follows. First, the variation in forest biomass, species bioRxiv preprint doi: https://doi.org/10.1101/2020.09.08.287938; this version posted September 9, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 87 richness and species properties were described using linear mixed-effects regression 88 models. These models accounted for the effects of environmental and human-related 89 variables, as well as sampling and biogeographical effects (see Methods and Figs. 3−7), 90 which explained 53% of the variation in biomass, 71% in species richness and 26−44% in 91 species properties (Supplementary Fig. 8, Supplementary Table 3). Next, we used these 92 models to generate baseline predictions in the absence of major human impacts, i.e., 93 predictions as if all sites were large, low-disturbance forest patches in landscapes with 94 100% of forest cover. We validated the precision of these predictions using simulations 95 (Supplementary Table 4). Finally, we defined an index of loss due to human-induced 96 impacts, defined as the standardized difference between observed values and baseline 97 predictions (Supplementary Fig. 9). Values of the index close to zero indicate little 98 human impact and the more negative the value, the greater the impact. 99 100 Results and discussion 101 Extent and magnitude of human impacts 102 We found that the majority of the Atlantic Forest surveys (83%) presented losses of 103 species richness and biomass (Fig. 1), i.e. negative indices of loss. These losses were 104 correlated with each other (Fig. 1), meaning that fragments that suffer greater losses of 105 biomass also lose more species. In absolute terms, human-induced impacts corresponded 106 to average declines of 23−32% of the richness and biomass relative to low-disturbance 107 Atlantic Forests (Table 1, Supplementary Table 5).
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