Integrating Ecosystem Management , Protected Areas , and Mammal Conservation in the Brazilian Amazon

The Amazon forest has been converted to a matrix of pristine and modified habitats. Landscape-scale biodiversity conservation requires an understanding of species’ distributions over this matrix to guarantee both effective protection and use for present and future generations. In this study, we evaluated how much of the existing and future planned protected areas (PAs) would be contributing to the conservation of Brazilian Amazon mammals (N = 399), including threatened species (N = 51). Currently, almost 37% of Brazilian Amazon is protected and that may increase to 46% if planned PAs are implemented. In the current PA system, 22% are indigenous land and 11% are sustainable use units, e.g., production forests. Only one-fifth of the whole range of mammal species occurring in Brazilian Amazon is actually protected by Brazilian PAs. However, considering only the part of the ranges within the Brazilian Amazon, and therefore under the scope of Brazilian actions, Brazilian PAs assume an important role in the protection of 39% of mammal distribution ranges, particularly the threatened species (39%). These results suggest that an integrated network of protected areas among Amazon countries would be necessary to increase their efficiency in mammal conservation. The need for strengthening of the forest sector and good management practices in Brazil appears critical for the maintenance of large extents of forest and species conservation. Under such a scenario, the contribution of developed nations and international agencies must assume an important role for the maintenance and enlargement of the protected area network in Amazon region.


INTRODUCTION
The advance of economic activities and their consequences for Amazon forests have been predicted and disseminated (Nepstad et al. 2001, Margulis 2003, Nepstad et al. 2004).The latest estimate of the deforestation rate for the Brazilian Amazon during the 2003-2004 period was 26,130 km2 (INPE 2005), almost half of the size of Costa Rica.This is the second highest deforestation rate recorded for Brazilian Amazon.Its causes are associated with cattle ranching, agriculture, and land speculation, with strong consequences to biodiversity conservation.
Landscape management and successful conservation strategies requires an understanding of species' distributions, including which species are restricted to protected areas and which could be adequately protected outside these areas.For slowing the advance of deforestation and conserving the high biological diversity of the region, the Brazilian government has, among other initiatives, invested in a network of protected areas on public lands.The Brazilian conservation units are divided in two main categories: areas of integral protection, e.g., parks, biological reserves, and areas for sustainable use, e. g., national forests, extractives reserves, and sustainable development reserves.In the former category, the use or harvest of natural resources for commercial purposes is not allowed.Besides these two types of protected areas, in public lands there http://www.ecologyandsociety.org/vol11/iss2/art17/are also indigenous lands and military areas.Although they are not considered conservation units by Brazilian law they also have restricted use, not been allowed any economical activities.For the purpose of this study, hereafter, conservation units, indigenous land and military areas are collectively called protected areas (PAs).In addition to the existing PAs, future conservation units are planned for the Brazilian Amazon.The Amazon Region Protected Areas (ARPA) project is a Brazilian government initiative for a system of 28.5 X 10 6 ha of parks and other protected areas, i.e., more than 10% of the Brazilian Amazon, to be implemented over 10 yr (www.mma.gov.br).ARPA also includes the consolidation of some already existing conservation units.It is coordinated by the Ministry of Environment and executed by the Brazilian Environmental Agency (IBAMA), with support from the World Bank, the World Wildlife Fund (WWF) pilot program for tropical forest protection in Brazil (PPG-7), the Global Environmental Facility (GEF), and the German Aid Agency (KFW).
According to Brazilian law, two of the main objectives of the National System of Conservation Units (SNUC; law 9985 of 18 July 2000) are, (1) the maintenance of biological and genetic resources, and (2) the protection of threatened species.To the best of our knowledge, those objectives have never been evaluated on a large scale for the whole network of protected areas, possibly due to the complexity involved in that operation.This evaluation becomes even more important nowadays as the choice of location and design of new protected areas is to be made and given the fact that, in the past, many protected areas were implemented for political reasons and not for their biological relevance.
In this study, we evaluated how much of the existing protected areas and the future planned areas would be contributing to the conservation of Brazilian Amazon terrestrial mammals.We used mammal distribution ranges as a first proxy for this analysis.Mammals are a well-known group, with reliable geographic information and generally used as flagship species to represent other groups.

METHODS
We performed a search on mammal occurrences and distribution ranges in Brazilian Amazonia using the NatureServe's InfoNatura databases as baseline (Patterson et al. 2003).Theses databases are a joint effort of the NatureServe, IUCN, and Conservation International, and were generated using published articles, reports, and expert inputs in several workshops.The output was species distribution maps, which are updated at least once a year.The maps provide a conservative estimate of the ranges as the methodology used probably results in an overestimation of the distribution area for some species.However, it is currently the best data available and also has the support and contribution of several mammal experts who participated in the workshops and continue to send their comments to update the databases.Therefore, we used these individual species distribution maps as the starting point of our analyses.
Mammal distribution ranges were superimposed on a map of the Brazilian Amazon and all species with part (> 1%) or all of their ranges within Brazilian Amazonia were selected.The Brazilian part of the range of selected species was then superimposed on a map of protected areas, and a map of the Amazon Region Protected Areas (ARPA).Subsequently, we recorded the percentage of overlap between species ranges and protected areas.This gave a general estimate of the potential effectiveness of the design, size, and location of protected areas (PAs) in protecting mammal species.We also performed analyses using a subset of these data, evaluating the case of threatened species.The list of threatened mammal species corresponds with the IUCN Red List.In a conservative approach, we also included in our analyses mammals in the "near-threatened" category.
We observed a high degree of overlap among PA boundaries.As there is no agreement related to the real contour of those areas yet, we had to assume an arbitrary criterion to remove these areas of overlap every time that occurred.Therefore, we first identified indigenous land boundaries, i.e., the most abundant, then, discounting areas of overlapping, we identified federal conservation units and, finally, state units.This step was important to avoid measuring the overlap between a mammal range and a PA twice in instances when a PA overlays another PA.http://www.ecologyandsociety.org/vol11/iss2/art17/

RESULTS
Currently, almost 37% of Brazilian Amazon is protected, when overlapping areas are removed (Fig. 1).Once implemented, the Amazon Region Protected Areas (ARPA) project would increase this percentage to 46% (Table 1).Indigenous lands (N = 355) occupy almost 21% of the Brazilian Amazon and are by far the most extensive PA network, followed by federal units, i.e., 9.3% of the area, state units (6.6%).Military areas (N = 20) cover only a small portion of the Brazilian Amazon (0.5%).The current overlap among different types of PAs may causes differences in area varying from 7.5% for state units to 49% for military areas (Table 1).
We recorded 399 mammal species for the entire Brazilian Amazon (Appendix).The overlap of their ranges generated a map, which indicated the areas with potential higher species richness (Fig. 2a).The western Amazon, the region along the Amazon River, and the north of Brazilian Amazon stand out as having the highest species richness.Overlaying PAs and military areas maps and this specie richness map allows a spatial visualization of the contribution of each unit in the conservation of mammal diversity (Fig. 2b-e; see details below).
In many cases, the range of a species exceeded the limits of the Brazilian Amazon and even of the Amazon basin.Therefore, we analyzed the contribution of Brazilian PAs considering this perspective.If we consider the whole distribution of a species, here called "Total range", or only the part their distribution comprising the Amazonia, "Panamazonia", the Brazilian PAs and military areas overlap with 18.7% and 24% of species ranges, respectively (Table 2).With ARPA implementation, that percentage may increase to 23% and 30%, respectively.The number of Brazilian mammal species that have at least a small part of their ranges inside a federal or state unit is considerable (N = 363 and 353, respectively).For indigenous land the number of mammals is slightly higher (N= 375).However, the mean proportion of their range within those units regarding their distribution in the Brazilian Amazonia is much lower than indigenous land (Table 2).Considering only part of the ranges effectively within the Brazilian Amazon boundaries, on average, 39% of mammal ranges are already protected within PAs and military areas, with 22% in indigenous lands, 10% in federal units, 7% in state units and 0.3% in military areas (Table 2).With the implementation of ARPA, almost 47% of mammal ranges would be included in PAs.
Among federal units, the percentage of overlapping between mammal ranges and areas of sustainable use (4.78%) or integral protection (4.76%) was very similar.On the other hand, among state units, areas of sustainable use exhibited a higher rate of overlapping (5.7%) than integrally protected areas (1.1%).Those differences have serious conservation implications as areas of sustainable use may have economic exploitation, e.g., extracting of timber, ecotourism, they demand a closer monitoring of impacts.
A similar approach can be used for subsets of the data or for species of special interest.Using as examples groups of mammals that normally receive the attention of conservationists, we observed that for 79 primate species found in the Brazilian Amazon, 28% of their whole range is contained within Brazilian PAs (Table 2).Considering just the part of the range within the Brazilian Amazon, almost 42% of their distribution ranges are included in PAs, i.e., 22% in indigenous land, 12% in federal units, and 8% in state units.The ARPA project would include another 10% of primate ranges, increasing the percentage of protected range to 53% (Table 2).Generally, primates have a more restricted range within the Amazon basin than, for instance, cats (N = 8), whose ranges overlapped 31% with PAs and military areas without ARPA and 38% with ARPA (Table 2).Small mammals, such as marsupials (N = 28), had 40% of their range contained in PAs, e.g., 19.7% in indigenous land, 8.5% in federal units, and 12% in state units.With ARPA (5%), this rate would increase to 45% (Table 2).
Overall, a total of 51 Brazilian Amazon mammal species are considered threatened based on IUCN red list, but only 22 species from those are in the Brazilian Environmental Agency (IBAMA) Red List.Considering their whole distribution range, the Brazilian PAs contributed to the protection of 18%, without ARPA, or 21%, with ARPA, of the total species ranges.Taking into account only part of the range within Brazilian Amazon boundaries, 39%, without ARPA, or 45%, with ARPA, of their ranges overlap with PAs (Table 2).
Considering all Brazilian mammal species, currently 263 species have from 31-50% of their ranges protected by some kind of PAs (Table 3).

DISCUSSION
For Amazon mammal species that occur in Brazil, less than one-fifth of their whole distribution range is protected under Brazilian Protected areas (PA) system.This shows that it is unlikely that only Brazilian PAs could protect Amazon mammal species.An integrated network of protected areas among Amazon countries appears necessary to increase the contribution of these areas to mammal conservation.For that, a similar analysis of this study should be done in neighboring Amazon countries to have a broader perspective of the protection status of some species.On the other hand, considering only the part of the ranges within Brazilian Amazon, and therefore under the scope of Brazilian actions, Brazilian PAs play an important role in the protection of 40% of mammal distribution ranges, including the threatened species (39%).
Indigenous lands, although not officially part of the conservation unit system, offer a great potential for the conservation of mammals, i.e., 22% of overlapping.As indigenous lands in Brazil occupy an area almost the size of Bolivia, they have a disproportional relevance in the conservation of fauna compared, for instance, to parks, which are 4 times smaller in size.Even though mammals are subjected to hunting in indigenous land, the potentially negative effect of this activity may be Ecology and Society 11(2): 17 http://www.ecologyandsociety.org/vol11/iss2/art17/Fig. 2. Map of richness of mammal ranges (N = 399) for Amazonia superimposed on main protected areas: federal conservation units, state conservation units, indigenous land, and Amazon Region Protected Areas (ARPA).The darker the color, the higher the richness.
Table 2. Percentage of overlap between mammal ranges and protected areas in the Brazilian Amazon, considering their total range, part of their ranges in Amazonia, i.e., "Panamazonia", and only part of their ranges in the Brazilian Amazon ("Braz.Amaz.").IL = indigenous land; FED = Federal units; ST = State units; MI = military areas.minimized given the size of these lands compared to the low density of the indigenous population.That may allow a rapid recovery of game species although we do need more research on this subject.

Groups
A recent study showed no difference regarding the inhibition of deforestation or fire between indigenous land and parks in Brazilian Amazon (Nepstad et al. 2006).The authors also concluded that as indigenous lands are usually located in areas of agricultural frontier expansion while parks are located in remote areas, the former would have an important role as barriers for deforestation and forest fires.
Federal and state units together include only 17% of the mammal ranges.That may be not enough for effective protection.Overall, sustainable use category, that which allows the performance of economic activities within its boundaries, comprises the largest amount of area (11%) compared to integral protection (6%), indicating the relevance of a good forest management to avoid species losses in those areas.Among these units, state units would be the most fragile regarding conservation not only because the sustainable use category occurs in higher number and size, but also because within this category, the models of use allow large economic and demographic use, e.g., "APA" area of environmental protection, but which may include an urban area.Also, it worth to notice that state units comprises a higher portion of threatened species ranges within their areas compared to federal units.
With the Brazilian government effort to increase PAs from 37-46% of Brazilian Amazon area in the next 10 yr, the protected fraction of mammal ranges would be 1.2 times larger than what already exists.That alone would already be extremely positive, but there is a chance that with the same size but better design and location of those areas, the biological relevance of these additional areas could be improved.For instance, detailed evaluations of other parameters, such as other taxa, the presence of species of interest, areas of higher richness, relevant environmental variables, and proximity to human communities may be used to decide between different types of categories of protection.
Additionally, it would be necessary to consider the impoverishment of forests due to logging (e.g., Azevedo-Ramos et al. 2005, 2006) and hunting within and outside the protected boundaries.Those actions would probably result in better conservation of an important fraction of Amazon fauna.The evaluation of these effects was beyond the objectives of this study, but they certainly need to be investigated for a better estimate of the status of protection of mammals in PAs and to better determine alternatives to mitigate the negative impacts.
Several parks, reserves, and indigenous land were analyzed for the direct and indirect effects of land use outside their boundaries.For instance, disturbances outside the protected limits can reduce by 15% the rainfall inside parks in tropical Africa (Roy et al. 2005).Plant richness of tropical forests is highly correlated to precipitation (Givnish 1999, Taplin andLovett 2003) and plants have great influence on the richness of other taxa (Kay et al. http://www.ecologyandsociety.org/vol11/iss2/art17/1997, Andrews and O'Brian 2000).Therefore, an evaluation of the influence of the surroundings on the ecosystem health of PAs is necessary to better guarantee the protection of biodiversity inside conservation units and indigenous land.For that and also to guarantee a largescale, integrated approach, it would be necessary to adopt a landscape approach as new management paradigm for PAs.
In a recent study that evaluated future scenarios of development for Panamazonia, we estimated that keeping the current trend of relatively little governance and increasing the infrastructure network, i.e., mainly roads, 30% of mammal species (N = 382) would have less than 60% of their range remaining due to accumulated deforestation until 2050 (Soares-Filho et al. 2006).The fact that currently, without ARPA, almost 61% of mammal ranges occur outside protected areas, reinforces the necessity of valuing forestry activities outside those boundaries that guarantee larger vegetation cover, larger and better ecological corridors, and genetic flux among population.With the implementation of ARPA, we would have 47% of mammal ranges within PAs.That demonstrates the importance of ARPA for a better protection of this group, but also indicates that actions that increase governance and better land use outside these units are of extreme importance to maximize the conservation of this animal group and biodiversity in general.
Environmentalists and the Brazilian government should keep this in mind, to distribute their efforts and resources proportionally.
The conservation of the current 37% or future 46% of Brazilian Amazon Forest within PAs is a monumental effort for a developing country like Brazil.The role of large forest areas, like the Amazon Basin, is of undeniable importance for global climate and the conservation of genetic resources.Deforestation in the Brazilian Amazon releases about 200 X 10 6 tons of C/yr, that is, 2-3% of total human emissions (Houghlton 2001).This increases to 10%, if emissions from logging and forest fire are included (Nepstad et al. 1999).
Additionally, one third of the global biodiversity is in Amazonia.
In this sense, the strengthening of the forest sector in Brazil as an economical alternative to ranching and agriculture becomes critical for the maintenance of large extents of forest.Also, new economic mechanisms taking advantages of the carbon market, such as compensated reduction of deforestation (Moutinho andSchwartzman 2005, Santilli et al. 2005), should not be underestimated as new economic sources for conservation.Of equal importance is the contribution of developed nations and international agencies for the maintenance and enlargement of these protected area networks.

Fig. 1 .
Fig. 1.Current and future planned protected areas (ARPA) in the Brazilian Amazon.

Table 1 .
Size (km 2 ) of protected areas (PAs) in the Brazilian Amazon with and without overlap with other units.PI = integral protection; US = sustainable use.

Table 3 .
Number of mammal species in different categories of range overlap with protected areas.