ECB-ART-46419
PeerJ
2018 Jan 01;6:e4869. doi: 10.7717/peerj.4869.
Show Gene links
Show Anatomy links
Primates in peril: the significance of Brazil, Madagascar, Indonesia and the Democratic Republic of the Congo for global primate conservation.
Estrada A
,
Garber PA
,
Mittermeier RA
,
Wich S
,
Gouveia S
,
Dobrovolski R
,
Nekaris KAI
,
Nijman V
,
Rylands AB
,
Maisels F
,
Williamson EA
,
Bicca-Marques J
,
Fuentes A
,
Jerusalinsky L
,
Johnson S
,
Rodrigues de Melo F
,
Oliveira L
,
Schwitzer C
,
Roos C
,
Cheyne SM
,
Martins Kierulff MC
,
Raharivololona B
,
Talebi M
,
Ratsimbazafy J
,
Supriatna J
,
Boonratana R
,
Wedana M
,
Setiawan A
.
Abstract
Primates occur in 90 countries, but four-Brazil, Madagascar, Indonesia, and the Democratic Republic of the Congo (DRC)-harbor 65% of the world''s primate species (439) and 60% of these primates are Threatened, Endangered, or Critically Endangered (IUCN Red List of Threatened Species 2017-3). Considering their importance for global primate conservation, we examine the anthropogenic pressures each country is facing that place their primate populations at risk. Habitat loss and fragmentation are main threats to primates in Brazil, Madagascar, and Indonesia. However, in DRC hunting for the commercial bushmeat trade is the primary threat. Encroachment on primate habitats driven by local and global market demands for food and non-food commodities hunting, illegal trade, the proliferation of invasive species, and human and domestic-animal borne infectious diseases cause habitat loss, population declines, and extirpation. Modeling agricultural expansion in the 21st century for the four countries under a worst-case-scenario, showed a primate range contraction of 78% for Brazil, 72% for Indonesia, 62% for Madagascar, and 32% for DRC. These pressures unfold in the context of expanding human populations with low levels of development. Weak governance across these four countries may limit effective primate conservation planning. We examine landscape and local approaches to effective primate conservation policies and assess the distribution of protected areas and primates in each country. Primates in Brazil and Madagascar have 38% of their range inside protected areas, 17% in Indonesia and 14% in DRC, suggesting that the great majority of primate populations remain vulnerable. We list the key challenges faced by the four countries to avert primate extinctions now and in the future. In the short term, effective law enforcement to stop illegal hunting and illegal forest destruction is absolutely key. Long-term success can only be achieved by focusing local and global public awareness, and actively engaging with international organizations, multinational businesses and consumer nations to reduce unsustainable demands on the environment. Finally, the four primate range countries need to ensure that integrated, sustainable land-use planning for economic development includes the maintenance of biodiversity and intact, functional natural ecosystems.
PubMed ID: 29922508
PMC ID: PMC6005167
Article link: PeerJ
Genes referenced: LOC100893907 LOC115925415 LOC583082 riok1
Article Images: [+] show captions
Figure 1. The richness of species and IUCN species conservation and population status of primates in Brazil, the Democratic Republic of the Congo (DRC), Madagascar and Indonesia.In the graph, the numbers below the names of the countries refer to the number of species used to calculate the percentages for species threatened and declining populations. Because population assessments are not available for all species, we focused on those for which recent information is available (Table S2). Source of data: IUCN Red List 2017-3 (http://www.iucnredlist.org; accessed 5 February 2018). | |
Figure 2. (A) Trends in tree cover loss (>30% canopy cover) in Brazil, DRC, Indonesia, and Madagascar for the period 2001–2016. (B) Cumulative tree cover (in Intact Forest Landscapes IFL) loss in each country for the same period. Source of data Global Forest Watch (http://www.globalforestwatch.org; accessed 5 February 2018). IFL: an unbroken expanse of natural ecosystems of at least 500 km2, forested, and without signs of significant human activity (Potapov et al., 2008). Forest loss ranged in Brazil from 2.74 M ha in 2001 to 5.37 M ha in 2016; in Indonesia from 745.43 K ha to 2.42 M ha; in DRC from 455.43 K ha to 1.38 M ha, and in Madagascar from 86.95 K ha to 383.55 K ha. | |
Figure 3. The projected expansion of agriculture and pastures in (A) Brazil, (B) the Democratic Republic of the Congo, (C) Madagascar, and (D) Indonesia for 2050 and 2100, under a worst-case scenario of land use from native vegetation to agricultural fields and pasture.See Text S1 for a description of the methods used. Data on species geographic distribution are derived from IUCN (2017) and the scenarios of agricultural expansion from the Integrated Model to Assess the Global Environment (IMAGE, version 2.2) (IMAGE Team, 2001) (see Dobrovolski et al., 2013). Notice the spatial shift of conservation conflicts, including the abandonment of some agricultural areas by 2100 in DRC and Madagascar. This condition, however, may not imply an immediate benefit for primate species, as local populations would have been extirpated, areas would have been dramatically altered prior to abandonment, and would likely require decades to regenerate to closed-canopy, old secondary forest. See Fig. S6 for a model based on an optimistic scenario and on a business-as-usual scenario. | |
Figure 4. Photos of selected land cover changes in primate range countries, illegal primate trade, and the primate bushmeat trade.Photo credits include the following: (A) Soybean plantation and recent deforestation of forest patches in the Cerrado Biome, Jataí, Goiás State, Brazil (Photo credit: Fabiano R. de Melo), (B) Pastures for cattle ranching surrounding Atlantic Forest patches inside the Cerrado Biome, Rio Verde, Goiás State, Brazil. (Photo credit: Izaltino Guimarães Jr), (C) Indonesia, illegal logging Central Kalimantan (Photo credit: R. Butler), (D) Indonesia, deforestation (Photo credit: R. Butler), (E) Indonesia, Sunda slow loris (Nycticebus coucang), sold in Jakarta (Photo credit: A. Walmsley and Little Fireface Project), (F) DRC, smoked bonobo (Pan paniscus) meat at a rural meat market (Photo credit: J. Head). | |
Figure 5. Total urban and rural population growth and projections for (A) Brazil, (B) DRC, (C) Madagascar, and (D) Indonesia.Steep growth is forecasted for the next few decades with urban populations significantly increasing, while rural populations are expected to decline. Source: http://www.fao.org/faostat/en/#data (accessed 15 August 2017). | |
Figure 7. The 1990–2015 Human Development Index (HDI) in Brazil, Indonesia, Madagascar, and DRC (Lowest human development = 0; highest = 1.0). Also shown is the average HDI for the world and for the top 25 most developed nations.The number in parentheses after each country indicates their HDI world rank. The number in parenthesis after the name of each country indicates its HDI ranking compared to 188 countries. No data are available for Madagascar for 1990. Source: United Nations Development Program (http://hdr.undp.org/en/composite/trend (accessed 11 January 2018). | |
Figure 8. The graph, produced using the World Bank database, shows the percentile rank of four key World Bank governance indicators for Brazil, DRC, Madagascar, and Indonesia. Percentile rank: the percentage of countries that rate below the selected country.Higher values indicate better governance ratings. Shown for comparison is the percentile rank for high-income OECD countries (n = 35; Organization for Economic Co-operation and Development). Percentile ranks have been adjusted to account for changes over time in the set of countries covered by the governance indicators. The statistically likely range of the governance indicator is shown as a thin black line. For instance, a bar of length 75% with the thin black lines extending from 60% to 85% has the following interpretation: an estimated 75% of the countries rate worse and an estimated 25% of the countries rate better than the country of choice. Source: http://info.worldbank.org/governance/wgi/index.aspx#reports (accessed 17 November 2017). | |
Figure 9. Distribution of protected areas and primate distributions in (A) Brazil, (B) DRC, (C) Madagascar, and (D) Indonesia.In this model, primate species distributions are based on data from the IUCN Red List (accessed May 2017), protected areas distributions from UNEP-WCMC (2017) and forest cover from Hansen et al. (2013). Images are scaled to ca. 300 m of spatial resolution. We included 2,190 protected areas in the Brazil dataset, 49 in DRC, 147 in Madagascar and 646 in Indonesia (Text S1). | |
Figure 10. Photos of selected primates from each country.Conservation status and photo credits include the following: (A) DRC, Grauer’s gorilla (Gorilla beringei graueri), Critically Endangered, (Photo credit: J. Martin), (B) Madagascar, Sahafary sportive lemur (Lepilemur septentrionalis) Critically Endangered (Photo credit: R. A. Mittermeier), (C) Indonesia, Javan slow loris (Nycticebus javanicus), Critically Endangered (Photo Credit: Andrew Walmsley/Little Fireface Project), (D) Brazil, northern muriqui (Brachyteles hypoxanthus), Critically Endangered (Photo credit: Raphaella Coutinho), (E) Brazil, pygmy marmoset (Cebuella pygmaea), Vulnerable, (Photo credit: Pablo Yépez), (F) Sumatran orangutan (Pongo abelii), Critically Endangered (Photo Credit: Perry van Duijnhoven). | |
Figure 11. Diagram summarizing key environmental challenges common to Brazil, DRC, Madagascar, and Indonesia that affect conservation of their primate fauna.The relative importance of some pressures and population aspects vary from country to country. For example, hunting in DRC is a large-scale pressure because the local human population has little or no access to domestic meat. Because of their large size and low population density relative to the size of the country, Brazil and DRC are in a better position to anticipate the direction of these pressures and prevent primate declines and extirpation. However, in contrast to Brazil, DRC is particularly poor, its human population is rapidly growing, and human development is very low, whereas civil unrest is predominant and corruption and weak governance are an ever-present condition. Madagascar differs from these two countries, and from Indonesia in having a very small percentage of its original forest left. A rapidly expanding human population and high levels of poverty and weak governance are predominant. Indonesia is a developing country with a large human population that has embarked on a policy of rapidly replacing its forests with commercial plantations and expanding industrial logging at the expense of biodiversity. |
References [+] :
Abernethy,
Extent and ecological consequences of hunting in Central African rainforests in the twenty-first century.
2013, Pubmed
Abernethy, Extent and ecological consequences of hunting in Central African rainforests in the twenty-first century. 2013, Pubmed
Alamgir, Economic, Socio-Political and Environmental Risks of Road Development in the Tropics. 2017, Pubmed
Alsamawi, The inequality footprints of nations: a novel approach to quantitative accounting of income inequality. 2014, Pubmed
Anne-Isola Nekaris, Tickled to death: analysing public perceptions of 'cute' videos of threatened species (slow lorises - Nycticebus spp.) on Web 2.0 sites. 2013, Pubmed
Banes, Reintroduction of confiscated and displaced mammals risks outbreeding and introgression in natural populations, as evidenced by orang-utans of divergent subspecies. 2016, Pubmed
Barrett, Luxury bushmeat trade threatens lemur conservation. 2009, Pubmed
Beaudrot, Standardized Assessment of Biodiversity Trends in Tropical Forest Protected Areas: The End Is Not in Sight. 2016, Pubmed
Bermejo, Ebola outbreak killed 5000 gorillas. 2006, Pubmed
Bernard, Downgrading, downsizing, degazettement, and reclassification of protected areas in Brazil. 2014, Pubmed
Brashares, Conservation policy. Wildlife decline and social conflict. 2014, Pubmed
Brodie, Bushmeat poaching reduces the seed dispersal and population growth rate of a mammal-dispersed tree. 2009, Pubmed
Brown, Shifting ranges and conservation challenges for lemurs in the face of climate change. 2015, Pubmed
Bublitz, Pathogenic enterobacteria in lemurs associated with anthropogenic disturbance. 2015, Pubmed
Burgess, Range contraction enables harvesting to extinction. 2017, Pubmed
Butler, New strategies for conserving tropical forests. 2008, Pubmed
Butt, Conservation. Biodiversity risks from fossil fuel extraction. 2013, Pubmed
Canale, Pervasive defaunation of forest remnants in a tropical biodiversity hotspot. 2012, Pubmed
Carlson, Effect of oil palm sustainability certification on deforestation and fire in Indonesia. 2018, Pubmed
Carrasco, Conservation. A double-edged sword for tropical forests. 2014, Pubmed
Caughlin, Loss of animal seed dispersal increases extinction risk in a tropical tree species due to pervasive negative density dependence across life stages. 2015, Pubmed
Ceballos, Mammal population losses and the extinction crisis. 2002, Pubmed
Courchamp, Rarity value and species extinction: the anthropogenic Allee effect. 2006, Pubmed
Crist, The interaction of human population, food production, and biodiversity protection. 2017, Pubmed
Dalerum, Identifying the role of conservation biology for solving the environmental crisis. 2014, Pubmed
Daszak, Emerging infectious diseases of wildlife--threats to biodiversity and human health. 2000, Pubmed
Dias, Translocation and radio-telemetry monitoring of pygmy marmoset, Cebuella pygmaea (Spix, 1823), in the Brazilian Amazon. 2015, Pubmed
Dolins, Conservation education in Madagascar: three case studies in the biologically diverse island-continent. 2010, Pubmed
Effiom, Bushmeat hunting changes regeneration of African rainforests. 2013, Pubmed
Estrada, Agroecosystems and primate conservation in the tropics: a review. 2012, Pubmed
Estrada, Impending extinction crisis of the world's primates: Why primates matter. 2017, Pubmed
Estrada, Socioeconomic contexts of primate conservation: population, poverty, global economic demands, and sustainable land use. 2013, Pubmed
Estrada, Primates in peril: the significance of Brazil, Madagascar, Indonesia and the Democratic Republic of the Congo for global primate conservation. 2018, Pubmed
Fa, Integrating sustainable hunting in biodiversity protection in Central Africa: hot spots, weak spots, and strong spots. 2014, Pubmed
Federman, Implications of lemuriform extinctions for the Malagasy flora. 2016, Pubmed
Garcia, Brazil's worst mining disaster: Corporations must be compelled to pay the actual environmental costs. 2017, Pubmed
Gouveia, Climate and land use changes will degrade the configuration of the landscape for titi monkeys in eastern Brazil. 2016, Pubmed
Gouveia, Functional planning units for the management of an endangered Brazilian titi monkey. 2017, Pubmed
Hansen, High-resolution global maps of 21st-century forest cover change. 2013, Pubmed
Hanski, Species-fragmented area relationship. 2013, Pubmed
Hilário, A primate at risk in Northeast Brazil: local extinctions of Coimbra Filho's titi (Callicebus coimbrai). 2017, Pubmed
Hoffmann, Persistent anthrax as a major driver of wildlife mortality in a tropical rainforest. 2017, Pubmed
Holden, High prices for rare species can drive large populations extinct: the anthropogenic Allee effect revisited. 2017, Pubmed
Hylander, The mechanisms causing extinction debts. 2013, Pubmed
Jenkins, Analysis of patterns of bushmeat consumption reveals extensive exploitation of protected species in eastern Madagascar. 2011, Pubmed
Joppa, High and far: biases in the location of protected areas. 2009, Pubmed
Kalamandeen, Pervasive Rise of Small-scale Deforestation in Amazonia. 2018, Pubmed
Kastner, Global changes in diets and the consequences for land requirements for food. 2012, Pubmed
Kauano, Illegal use of natural resources in federal protected areas of the Brazilian Amazon. 2017, Pubmed
Latrubesse, Damming the rivers of the Amazon basin. 2017, Pubmed
Laurance, Estimating the Environmental Costs of Africa's Massive "Development Corridors". 2015, Pubmed
Laurance, Agricultural expansion and its impacts on tropical nature. 2014, Pubmed
Lewis, Increasing human dominance of tropical forests. 2015, Pubmed
Longa, Human herpesvirus 1 in wild marmosets, Brazil, 2008. 2011, Pubmed
Malhi, Climate change, deforestation, and the fate of the Amazon. 2008, Pubmed
McGuire, FAO, IFAD, and WFP. The State of Food Insecurity in the World 2015: Meeting the 2015 International Hunger Targets: Taking Stock of Uneven Progress. Rome: FAO, 2015. 2015, Pubmed
Meijaard, Quantifying killing of orangutans and human-orangutan conflict in Kalimantan, Indonesia. 2011, Pubmed
Meyer, Assessing the exposure of lion tamarins (Leontopithecus spp.) to future climate change. 2014, Pubmed
Nekaris, Exploring cultural drivers for wildlife trade via an ethnoprimatological approach: a case study of slender and slow lorises (Loris and Nycticebus) in South and Southeast Asia. 2010, Pubmed
Nekaris, A novel application of cultural consensus models to evaluate conservation education programs. 2018, Pubmed
Nepstad, Slowing Amazon deforestation through public policy and interventions in beef and soy supply chains. 2014, Pubmed
Newmark, Targeted habitat restoration can reduce extinction rates in fragmented forests. 2017, Pubmed
Nijman, Orangutan trade, confiscations, and lack of prosecutions in Indonesia. 2017, Pubmed
Nijman, Changes in the primate trade in indonesian wildlife markets over a 25-year period: Fewer apes and langurs, more macaques, and slow lorises. 2017, Pubmed
Overbeck, Global Biodiversity Threatened by Science Budget Cuts in Brazil. 2018, Pubmed
Pacheco, Genetic Structure of a Mimosoid Tree Deprived of Its Seed Disperser, the Spider Monkey. 2000, Pubmed
Peres, Dispersal limitation induces long-term biomass collapse in overhunted Amazonian forests. 2016, Pubmed
Pigott, Updates to the zoonotic niche map of Ebola virus disease in Africa. 2016, Pubmed
Pigott, Mapping the zoonotic niche of Ebola virus disease in Africa. 2014, Pubmed
Plumptre, Catastrophic Decline of World's Largest Primate: 80% Loss of Grauer's Gorilla (Gorilla beringei graueri) Population Justifies Critically Endangered Status. 2016, Pubmed
Potapov, The last frontiers of wilderness: Tracking loss of intact forest landscapes from 2000 to 2013. 2017, Pubmed
Rasambainarivo, Survey of Giardia and Cryptosporidium in lemurs from the Ranomafana National Park, Madagascar. 2013, Pubmed
Robbins, Extreme conservation leads to recovery of the Virunga mountain gorillas. 2011, Pubmed
Rovero, Primates decline rapidly in unprotected forests: evidence from a monitoring program with data constraints. 2015, Pubmed
Runting, Alternative futures for Borneo show the value of integrating economic and conservation targets across borders. 2015, Pubmed
Santika, First integrative trend analysis for a great ape species in Borneo. 2017, Pubmed
Schillaci, Exposure to human respiratory viruses among urban performing monkeys in Indonesia. 2006, Pubmed
Schloss, Dispersal will limit ability of mammals to track climate change in the Western Hemisphere. 2012, Pubmed
Schwitzer, Conservation. Averting lemur extinctions amid Madagascar's political crisis. 2014, Pubmed
Shanee, Diagnostic overview of the illegal trade in primates and law enforcement in Peru. 2017, Pubmed
Soedarmanto, Identification and molecular characterization of serological group C streptococci isolated from diseased pigs and monkeys in Indonesia. 1996, Pubmed
Sonter, Mining drives extensive deforestation in the Brazilian Amazon. 2017, Pubmed
Spracklen, A Global Analysis of Deforestation in Moist Tropical Forest Protected Areas. 2015, Pubmed
Strassburg, Moment of truth for the Cerrado hotspot. 2017, Pubmed
Strier, Demographic monitoring of wild muriqui populations: Criteria for defining priority areas and monitoring intensity. 2017, Pubmed , Echinobase
Strindberg, Guns, germs, and trees determine density and distribution of gorillas and chimpanzees in Western Equatorial Africa. 2018, Pubmed
Struebig, Anticipated climate and land-cover changes reveal refuge areas for Borneo's orang-utans. 2015, Pubmed
Svensson, Disappearing in the Night: An Overview on Trade and Legislation of Night Monkeys in South and Central America. 2016, Pubmed
Tanentzap, Resolving Conflicts between Agriculture and the Natural Environment. 2015, Pubmed
Taubert, Global patterns of tropical forest fragmentation. 2018, Pubmed
Tilman, Future threats to biodiversity and pathways to their prevention. 2017, Pubmed
Tilman, Global diets link environmental sustainability and human health. 2014, Pubmed
Timpe, The changing hydrology of a dammed Amazon. 2017, Pubmed
Venter, Reducing emissions from deforestation and forest degradation (REDD+): game changer or just another quick fix? 2012, Pubmed
Venter, Targeting global protected area expansion for imperiled biodiversity. 2014, Pubmed
Voigt, Global Demand for Natural Resources Eliminated More Than 100,000 Bornean Orangutans. 2018, Pubmed
Waeber, How Effective Have Thirty Years of Internationally Driven Conservation and Development Efforts Been in Madagascar? 2016, Pubmed
Wich, Understanding the impacts of land-use policies on a threatened species: is there a future for the Bornean orang-utan? 2012, Pubmed
Wich, Will oil palm's homecoming spell doom for Africa's great apes? 2014, Pubmed
Wiederholt, Tropical warming and the dynamics of endangered primates. 2010, Pubmed
Wilson, Conservation strategies for orangutans: reintroduction versus habitat preservation and the benefits of sustainably logged forest. 2014, Pubmed
Winemiller, DEVELOPMENT AND ENVIRONMENT. Balancing hydropower and biodiversity in the Amazon, Congo, and Mekong. 2016, Pubmed
Wolf, Range contractions of the world's large carnivores. 2017, Pubmed
Zelazowski, Changes in the potential distribution of humid tropical forests on a warmer planet. 2011, Pubmed
de Almeida, Yellow fever outbreak affecting Alouatta populations in southern Brazil (Rio Grande do Sul State), 2008-2009. 2012, Pubmed