107– 10.3897/natureconservation.22.13823 Biodiversity, threats and conservation challenges in the Cerrado of Amapá, an Amazonian savanna

An Amazonian savanna in northern Brazil known as the Cerrado of Amapá is under imminent threat from poor land-use planning, the expansion of large-scale agriculture and other anthropogenic pressures. These savannas house a rich and unique flora and fauna, including endemic plants and animals. However, the area remains under-sampled for most taxa, and better sampling may uncover new species. We estimate that only ~9.16% of these habitats have any kind of protection, and legislative changes threaten to further weaken or remove this protection. Here we present the status of knowledge concerning the biodiversity of the Cerrado of Amapá, its conservation status, and the main threats to the conservation of this Amazonian savanna. To secure the future of these unique and imperilled habitats, we suggest urgent expansion of protected areas, as well as measures that would promote less-damaging land uses to support the local population.


Introduction
Tropical savannas are dynamic systems of grassland and open woodland that cover 15 to 24.6 million km 2 of South America, Africa and Asia (Silva and Bates 2002), occupying one-fifth of the Earth's surface (Scholes and Archer 1997). A large part of the human population lives and works within these ecosystems, which house more pastoral land and wild herbivores than any other in the world, and which have a significant impact on the global economy (Sankaran et al. 2005;Scholes and Archer 1997). Tropical savannas are also recognised globally for their rich and unique biodiversity, and this, together with high levels of anthropogenic disturbance, has led to increasing conservation concern (e.g. Klink and Machado 2005). In South America, the largest savanna complexes are the Cerrado in Brazil, Bolivia and Paraguay, and the Llanos in Venezuela and Colombia (Silva and Bates 2002). However, further islands of savanna of varying size occur throughout the Amazon biome, known as Amazonian savannas (Carvalho and Mustin 2017;Prance 1996). The Amazonian savannas represent a distinct ecosystem within the large Amazonian region (see Prance 1996), different also from the white-sand ecosystems that further pepper the Amazon biome (see Adeney et al. 2016). These Amazonian savannas have generally been under-studied (see Carvalho and Mustin 2017) and are highly threatened, principally as a result of landgrabbing and the advance of cultivation of grãos (grains and pulses, mainly soybeans and maize), plantations of exotic woody species (eucalyptus and acacia), and uncontrolled fires (Barbosa et al. 2007;Carvalho and Mustin 2017;Aguiar et al. 2014).
It has been estimated that, in Brazil,12.3% of Amazonian savannas are within Strictly Protected areas (IUCN categories I-IV), 5.1% in Multiple Use areas (IUCN categories V-VI) and 40.3% in Indigenous Lands (Carvalho and Mustin 2017). Indigenous Lands have been shown to be effective in preventing deforestation (Nepstad et al. 2006), however, the effectiveness of protected areas in preventing degradation depends not only on protection type but also on the level of anthropogenic pressure to which the areas are exposed, and the intensity of enforcement among other factors (Nolte et al. 2013;Pfaff et al. 2014). Furthermore, some types of multiple use areas can offer protection of both biodiversity and local communities in the face of large-scale development, but it should not be assumed that local needs, expectations and attitudes toward conservation are easily compatible with conservation goals (Kohler and Brondizio 2017).
In recent years, a lack of protection of less isolated areas of Amazonian savannas (Cerrado of Amapá, Lavrados of Roraima and smaller fragments including those at Humaitá, Santarém and Monte Alegre), has facilitated the opening up of new areas to plantations of grãos and associated degradation of savanna areas (Barbosa 2013; Barbosa and Campos 2011;Carvalho and Mustin 2017;Vidal 2017). Since 2006, deforestation of Amazonian forests to make way for soybean plantations has declined considerably, thanks largely to the implementation of a moratorium on soya (Gibbs et al. 2015). However, the expansion of soybean cultivation in Brazil has shifted the agricultural frontier to other areas such as the region between the states of Maranhão, Piauí, Tocantins, and Bahia, known as MAPITOBA, and has maintained its expansion across the Cerrado (Gibbs et al. 2015). The moratorium on soya is not applicable in the Cerrado biome, and is also seemingly not being applied to savanna habitats within the Amazon, opening up these areas to large-scale production of grãos. This can lead to deforestation and degradation, conservation conflicts and conflicts over land, increased burning and displacement of traditional populations (Barbosa 2013;Barbosa et al. 2007;Domingues and Bermann 2012;Fearnside 2006;Gibbs et al. 2015;Vidal 2017).

The Cerrado of Amapá
The Cerrado of Amapá is one of the largest, least protected and arguably the most threatened complexes of Amazonian savanna in Brazil at present (see Carvalho and Mustin 2017). It covers approximately ~7.2% of the total area (~140,012 km 2 ) of the state of Amapá, in the far north of Brazil. Amapá has no road connections to the rest of the country and has very limited connections with neighbouring French Guiana. These facts have doubtless contributed to protecting the Cerrado of Amapá from large-scale agricultural activities until now. However, the state does have a port at the mouth of the Amazon River that allows for export of grãos, wood and minerals to China (via the Panama Canal) and Europe (Monteiro 2015).
The Cerrado of Amapá is characterised by a mosaic of areas with open woody vegetation, areas with a denser woody shrub layer, and open grassy areas with sparser shrubs and trees, and by seasonally flooded areas in the transition zone with floodplains (Castro 2009;Mochiutti and Meirelles 1994;Oliveira 2009). This ecosystem is also intersected by gallery forests (Castro 2009;Mochiutti and Meirelles 1994). The Cerrado of Amapá can be subdivided in to areas dominated by one of four main vegetation types: shrub savanna (savana arborizada), woodland savanna (savana florestada), grass savanna (savana gramíneo-lenhosa) and park savanna (savana parque) (Figures 1 and   2). There is clear variation in the composition and number of species that can be encountered in different locations in the Cerrado of Amapá. For example, the woody species Salvertia convallariodora is not found in the savanna areas to the north of the Araguari River, despite being one of the most abundant species in the savannas to the south of this same river (GEA et al. 2016).  The Cerrado of Amapá is among the most threatened ecosystems in the state (IBGE 2004b) and is subject to high human pressure containing both the largest urban centres and the majority of the network of highways of the state (see Figure 3). Since 2004 it has been recognised as a "very high" conservation priority for Brazil (Brazil 2004).
Despite this recognition, and despite representing ~7% of the area of the state, as well as a significant percentage of its economically productive area, the Cerrado of Amapá has not received the attention that we argue it deserves. Here we present the status of knowledge concerning the biodiversity of the Cerrado of Amapá, its conservation status, and the main threats to the conservation of this Amazonian savanna. We further suggest pathways necessary to conserve this unique ecosystem and to secure its future in the face of mounting anthropogenic threats.  Schunck et al. 2011;Silva et al. 2013;Silva et al. 1997;Silva et al. 2006;Silveira 2003; Silva et al. 2015). The species Philodendron carinatum E.G.Gonç., also found in the Cerrado of Amapá, is considered rare in Brazil (Temponi et al. 2009). Amphibian species richness is high relative to other Amazonian savannas, likely maintained by the complex mosaic of savanna, forest patches, swamps and temporary ponds (Lima et al. 2017). Two fish species have also been described from the Cerrado of Amapáthe Amapá tetra Hyphessobrycon amapaensis (Zarske and Géry 1998), and Melanorivulus schuncki (Costa and De Luca 2010). The Amapá tetra has a very restricted distribution, and as such maintaining the integrity of the streams in which it is found is extremely important for the conservation of this species (Nogueira et al. 2010). At least two of the mammals that have been recorded are endemic to the Amazonian savannas -Alston's cotton rat Sigmodon alstoni and a recently discovered species of opossum Cryptonanus sp. (Silva et al. 2013;Voss 2015). However, the area remains under-sampled for most taxa, and new state records of species of amphibians, birds and mammals have been made in the Cerrado of Amapá (Costa-Campos and Freire 2015;Schunck et al. 2011;Silva et al. 2013;Silva et al. 1997), highlighting the possibility of encountering new species and/or extending the ranges of existing species with better sampling of the region.
Owing to its geographic isolation and therefore relatively well-preserved state, Amapá is particularly important for the conservation of some species. For example, the only known populations of red-handed howler monkey (Alouatta belzebul) to the north of the Amazon River are found in the state of Amapá, where preliminary surveys show that occurrence of this species is predominantly limited to riparian forest within the Cerrado of Amapá (R. Hilário, unpublished data). To the south of the Amazon River, most populations of this species are highly threatened by the arc of deforestation, with just 10 small populations of this species remaining outside of the main area of deforestation pressure, in the Northeast Region of Brazil (Veiga et al. 2008). The species is listed as  2016). Importantly, E. rufomarginatus was previously listed as vulnerable, and was down-graded specifically due to its presence outside the highly threatened Cerrado biome, in the Amazonian savannas (IUCN 2016). As such, the massive conversion of the Cerrado of Amapá for agricultural production would represent a substantial loss of important habitat for E. rufomarginatus, and the species would almost certainly be upgraded once more in the IUCN Red List.

Conservation status
While the state of Amapá has ~72% of its territory covered by protected areas (Dias et al. 2016), these areas are almost entirely made up of terra firme (lowland tropical forest) and várzea (floodplain) forests, and flooded areas, and just 917.69 km 2 (~9.16%) of the Cerrado of Amapá has protection in strictly protected areas, multiple use areas and Indigenous Lands (Table 1). At least an additional 68.9 -274.9 km 2 of savanna habitats fall within quilombos, traditional lands of the descendants of escaped African slaves, which are recognised under Brazilian Federal law as protected areas (Brazil 2006).
However, biodiversity conservation is not usually a primary objective of these areas and their effectiveness in protecting against degradation has not been well documented. The vast majority of protected savanna habitats in Amapá are within multiple use or sustainable use areas (IUCN category V-VI; 850.42 km 2 , 8.49% of the total area) ( Table   1).
Protection also varies across the four dominant vegetation types. For example, the grass savannas, the second most common savanna type in the Cerrado of Amapá, are the least protected, with just 1.19% of their 930.22 km 2 falling within the Amapá State Forest, a multiple use area (Table 1) PAs, and about two-thirds of the shrub savannas that have protection (Table 1). As such, were it to be down-sized or degazetted, the grass savannas and woodland savannas of the Cerrado of Amapá could lose all protection, and shrub savannas could have their protection substantially reduced.
Park savannas represent ~60% of the total area of the Cerrado of Amapá, and are the only dominant vegetation type to be protected outside of multiple use areas (Table 1).
However, most of their protection is still offered by multiple use areas including the Amapá state forest, the Rio do Cajari Extractive Reserve, and the Curiaú Environmental Protection Area (Table 1). Environmental Protection Areas (APAs), such as Curiaú, are not, however, subject to the same environmental licensing requirements for activities that have the potential to be polluting or to cause environmental degradation that govern other conservation units in Brazil (Brazil 2011 Approximately 40 km 2 of park savanna is also protected by strictly protected areas -the Cabo Orange National Park and the Seringal Triunfo Private Reserve (Table 1), and a further ~27 km 2 fall within the Uaça Indigenous Land (Table 1). There is an overlap between Cabo Orange National Park and the Cunani Quilombo and owing to conflicting legislation, negotiations are on-going regarding the limits of the two protected areas which could eventually lead to a reduction in the amount of savanna habitat under strict protection. In Brazil, Indigenous Lands offer very effective protection (Nepstad et al. 2006), but the Brazilian federal government is currently considering modifications to legislation that would allow for exploitation of natural resources within Indigenous Lands (Fearnside 2016). As such, should the legislation be approved, Indigenous Lands could be opened up to mining and large-scale planting of crops (Fearnside 2016).
Taking all of this into consideration, we conclude that the Cerrado of Amapá does not currently have effective long-term protection.

Major threats: present and future
While there is no good estimate available of the total area of the Cerrado of Amapá that has been cleared and/or degraded, estimates suggest that at least 450 km 2 have been cleared (Sano et al. 2017), and one estimate does suggest that up to ~1,949 km 2 (~19.5% of the total area) have been altered for use in silviculture, mechanized agriculture, livestock production and exploration of mineral resources (GEA et al. 2016). This Obvious exceptions to this pattern are Ferreira Gomes and Porto Grande, which is probably a reflection of the replacement of much of the savanna habitats in these municipalities with plantations of eucalyptus and acacia (see Figures 1 and 4), where fires are controlled by the companies that administer these plantations. While fire in Amazonian savannas has been present since pre-Columbian times, as indicated by charcoal in the soil (e.g. Turcios et al. 2016), these clear increases in recent years could be driven by climatic influences or by the expansion of commercial agriculture in some municipalities. Indeed, expansion of agriculture and livestock production across the state is likely to aggravate this threat, and in turn lead to a loss of biodiversity from the Cerrado of Amapá. The presence of roads, and consequent ignition sources, dramatically increases the frequency of fires in Amazonian savannas (Barbosa and Fearnside 2005b) and the Cerrado of Amapá contains more than half of the inter-city highways in the state (Figure 3).  Ecological-Economic Zoning (Brazil 2002). To allow for the identification of representative areas for the protection of the region's biodiversity, investment of resources in research is now urgently required. Indeed, while many parts of the Cerrado of Amapá remain under-sampled, it is already clear that much heterogeneity exists in the flora and fauna of these savannas. As such, implementation of new protected areas within the Cerrado of Amapá must now be guaranteed, and these PAs must be positioned to be representative of the savanna ecosystem, taking in to account this heterogeneity and the social value of the different areas (Fearnside 2015;Fearnside and Ferraz 1995). Without such a process, there is a risk of losing a unique and important biodiversity before it has been properly documented.
Other priorities for sustainable development of the Cerrado of Amapá should include implementation of sustainable management practices, including appropriate management of the fire regime (Borges et al. 2016), soil conservation measures (Hudson 1995) and reduced pesticide and herbicide usage (Grovermann et al. 2017).
Mechanisms should also be put in place to protect the many freshwater springs that originate in, or feed into, the Cerrado of Amapá. Crucially, proper monitoring will be required to evaluate the impacts of all activities in these unique savanna habitats, and particularly to ensure that negative biodiversity and social impacts of large-scale intensive agriculture and plantations are minimised. Indeed, sustainable development in the region will be impossible without a planning approach that generates income to sustain local rural populations (Dias et al. 2016). Mechanisms that support and favour the continued development of markets and incentives for small-scale producers will be crucial for the sustainable development of the state of Amapá. At a broader scale, we further highlight the need to recognise the Amazonian savannas as a distinct and important habitat type, different from others large areas of savannas (i.e. Brazilian Cerrado), which would allow specific conservation initiatives to be implemented as part of a broader conservation policy. For example, Brazil's soya moratorium, which requires that soybeans not be produced in Amazonian forest areas deforested after July 2006 (Gibbs et al. 2015), could and should now be extended to require the same of soybeans produced in areas of Amazonian savanna (see Carvalho and Mustin 2017).
Productivity could be increased through integrated crop-livestock-forest systems (ICLFS) in areas already planted with eucalyptus. ICLFS contribute to soil conservation, using the soil more intensively but in concert with ecological management tools such as direct planting (Moraes et al. 2014). This type of approach to increase productivity has been promoted as a form land sparing to prevent the loss of stored carbon under the assumption that new areas will not be opened for agriculture (Pacheco et al. 2013). Brazil's voluntary pledges at the 2005 15 th Conference of the Parties of the climate convention (COP-15) include the use of technologies such as ICLFS to help cut carbon emissions (Kichel et al. 2014). Brazil's Low-Carbon Agriculture (ABC) programme was launched in 2010 (Brazil 2010), and this programme further incentivizes implementation of ICLFS through provision of low-interest loans, although uptake has been slow (Angelo 2012;Strassburg et al. 2014). However, land sparing is a difficult conservation strategy because financial success of more productive commercial agriculture leads to more, rather than less, clearing for agricultural expansion (e.g. Fearnside 1987;Kaimowitz and Angelsen 2008).
Avoiding the conversion of Amazonian savannas to agriculture would contribute to maintaining climatic stability at local and regional scales (Butt et al. 2011) and benefit biodiversity conservation. The roots of savanna vegetation store a significant quantity of below-ground carbon (Barbosa et al. 2012). Without an effective programme to avoid savanna conversion, the quantity of carbon released by the savannas of Amapá could reach 8.15 t ha -1 [estimate based on data from arboreal vegetation near Macapá collated by JJT and estimates available for Roraima according to from Barbosa and Fearnside (2005a) and Barbosa et al. (2012)]. This release would represent a loss of US$ 27 ha -1 , since each ton of carbon could be sold for US$ 3.30 in the Voluntary Carbon Market (Hamrick and Goldstein 2016).
Here we draw attention to the Cerrado of Amapá, a biodiverse and highly threatened ecosystem that has to date received very little attention and almost no protection, compared with forested parts of the state. We have shown that there is an urgent need to implement protected areas, with local communities, scientists, conservationists and policy-makers working together to construct a sustainable and equitable plan for their management. By doing so, we can ensure the sustainable development of this isolated state in the far north of Brazil, providing solutions that result in positive social, economic and biodiversity outcomes-the so-called 'triple bottom line' for conservation.