Conservation Status and Challenges of the Atlantic Forest Birds of Paraguay

: The Atlantic Forest, one of the most biodiverse biomes in the world, is also one of the most endangered. In Paraguay, its remnants are mostly fragmented and isolated. The Paraguay Biodiversity Corridor is an initiative that is being developed to generate and maintain connectivity of the main conservation areas. With the objective to analyze the bird richness and occurrence in each of the core areas of this corridor, we gathered published data, details of the management plans, and bird surveys recorded during 2015 and 2017 in these areas. In total, 557 bird species occur in the core areas of the Corridor, representing more than 80% of the birds of the country. San Rafael National Park and Mbaracay ú Forest Nature Reserve are the richest areas, with 427 (70) and 408 (61) bird species (Atlantic forest endemics), respectively. These two areas also harbor more than 30 bird species of global conservation concern. Only 24% of the Corridor area is protected or sustainably managed, with only 10% under strict protection. The Corridor situated within this endangered biome encompasses some of the most important areas for bird conservation, but the situation of many of these areas is alarming as they are not protected or e ﬀ ectively managed to conserve their biodiversity. Restoration of connectivity, legal enforcement, and strengthening of authorities to combat deforestation on core areas, along with research focused on the impact contributed by human activities (selective logging, ecotoxicity exposure to agrochemicals) are key actions prioritized for the Upper Parana Atlantic forest (UPAF) Corridor.


Introduction
The Atlantic forest of South America has been identified as one of the most important biodiversity hotspots of the planet. It is a complex of 15 terrestrial eco-regions of tropical and sub-tropical humid forests [1] with the highest concentration of plant and vertebrate endemism. With only 8% of its original extent remaining as a consequence of the degradation imposed by human activities, today, this ecoregion is considered one of the most endangered biomes [2,3]. Originally, the forest covered one tenth of the south American continent, extending from Río Grande do Norte and Ceará south to Río Grande do Sul in Brazil, Northeast of Argentina and east of Paraguay, with a total of 1,233,875 km 2 [3]. In Paraguay, the Upper Parana Atlantic forest (UPAF) eco-region encompasses more than 88,000 km 2 . It was almost "intact" until 1940, its degradation being mainly due to selective

Historical Bird Records
We have compiled all previous studies, reports, or published materials at each study site in order to obtain a total of bird species recorded in each site (Table 1).

Bird Counts and Richness Estimators
We conducted 10-min unlimited-distance point counts [35] at available trails at 15 core areas ( Table 2). On each trail, counts stations were located at least 200 m apart, and more than 100 m away from the forest edge. Point counts were conducted from 30 min before sunrise (in order to record nocturnal and crepuscular species) to 3 h after sunrise. We recorded each bird or group of birds detected aurally or visually. No counts were conducted on rainy or windy days, and all counts were made by the same observer (A.E.).
Due to difference in bird count efforts, we analyzed data clustering point counts in some areas as defined in Table 2. Species-accumulation curves and species richness estimators were computed using EstimateS, version 9.1.0 [36]. We used sample-based incidence data randomizations of the clustering point counts. In each randomization, sampled species were drawn randomly from the data set without replacement and added to the curve in a random order. We used 100 runs of randomized sampling order and extrapolated the rarefaction curves to a total of 500 samples. Table 2. Designation of grouped core areas to analyze point count data in order to estimate richness of bird species at the Paraguay Biodiversity Corridor.

Bird Richness at the Paraguay Biodiversity Corridor
A total of 200 bird species were recorded during 318 10-min point counts surveyed in the core areas of the corridor. In average, 11.6 (range = 1-24) bird species were recorded during point counts, being higher at Agropeco (15.2 species), Kanguery (14.2), and Tapyta (14.2; Table 4). Species accumulation curves for grouped core areas (see Section 2.3) of all bird species recorded during 318 10-point count stations showed that estimation of bird richness did not depend on sample efforts, as bird richness estimation for some areas were higher even with lower number of samples than others. Bird richness obtained through an extrapolation to 500 counts for each grouped core area, estimated for Kanguery (center of the reserve) 163.5 (95% C.I. = 111.4-215.5) bird species with a sample of only 26 10-min point counts, while at south of San Rafael it is estimated to be 122.4 (103.9-140.9) with a total of 72 10-min point counts ( Figure 2). during 318 10-point count stations showed that estimation of bird richness did not depend on sample efforts, as bird richness estimation for some areas were higher even with lower number of samples than others. Bird richness obtained through an extrapolation to 500 counts for each grouped core area, estimated for Kanguery (center of the reserve) 163.5 (95% C.I. = 111.4-215.5) bird species with a sample of only 26 10-min point counts, while at south of San Rafael it is estimated to be 122.4 (103.9-140.9) with a total of 72 10-min point counts ( Figure 2). Corridor. Total number of counts for each core grouped areas is extrapolated to 500 samples.

Endemic Species at the Paraguay Biodiversity Corridor
Eighty-seven species out of the 557 registered in the Paraguay Biodiversity Corridor are endemic to one of the ecoregions that occur in the country. Total number of counts for each core grouped areas is extrapolated to 500 samples.

Endemic Species at the Paraguay Biodiversity Corridor
Eighty-seven species out of the 557 registered in the Paraguay Biodiversity Corridor are endemic to one of the ecoregions that occur in the country.
The 78 endemic species of the UPAF are present within the Paraguay Biodiversity Corridor, which demonstrates the importance of the Protected Areas for the conservation of the biodiversity of this ecoregion. The core areas with the highest number of endemic species are: San Rafael National Park (70 species), Itabó Biological Reserve (66 species), Tapyta Private Nature Reserve (65 species), Caazapá National Park (64 species), and Mbaracayú Forest Nature Reserve (61 species; Table 3).
In the Corridor, five of the 11 Cerrado endemic species of the country, two of 17 Chaco endemics, and two Mesopotamian Grasslands endemic species have been recorded in the core areas.

Endemic Richness at the Paraguay Biodiversity Corridor
A total of 52 Atlantic forest endemic species were recorded during 318 10-min point counts surveyed in the core areas of the corridor. In average, 3.8 (range = 0-11) endemic species were recorded during point counts, being higher at Agropeco (5.3 species), Tapyta (4.8), and south of San Rafael (4.5; Table 5). Sample effort did affect species accumulation curves of Atlantic forest endemic bird species, showing higher richness with increase of sample efforts, expect for Itaipu, in which the reduce number of point counts is not enough for a robust estimation. The two grouped core areas with highest number of point counts, Ypeti Private Nature Reserve (68 point counts), and south of San Rafael (72 point counts) yield higher endemic richness, with 55.4 (95% CI = 30.8-79.9) and 52.6 (95% CI = 21.4-83.7), respectively ( Figure 3). Sample effort did affect species accumulation curves of Atlantic forest endemic bird species, showing higher richness with increase of sample efforts, expect for Itaipu, in which the reduce number of point counts is not enough for a robust estimation. The two grouped core areas with highest number of point counts, Ypeti Private Nature Reserve (68 point counts), and south of San Rafael (72 point counts) yield higher endemic richness, with 55.4 (95% CI = 30.8-79.9) and 52.6 (95% CI = 21.4-83.7), respectively ( Figure 3).   Table 3).
Forty-two percent (21 species) out of the 50 species with global conservation issues are endemic to the Upper Paraná Atlantic Forest. Twelve endemic species are Near Threatened with extinction, six are Vulnerable, two are Endangered and one is Critically Endangered ( Table 6).
Among the Near Threatened species, the Mantled Hawk (Pseudastur polionotus) has only been recorded at the Carapá Nature Reserve; the Rusty-barred Owl (Strix hylophila) at three protected areas: San Rafael National Park, Maharishi Nature Reserve, and Itabó Biological Reserve; the White-browed Foliage-gleaner (Anabacerthia amaurotis) has also been recorded at only three protected areas: San Rafael National Park, Ypeti Nature Reserve, and Caazapá National Park.
Among the Vulnerable species, the Red-spectacled Amazon (Amazona pretrei) is only known from a historical record at Itabó Biological Reserve; the Buffy-fronted Seedeater (Sporophila frontalis) at the Ybytyruzu Management Reserve and the Tapyta Private Nature Reserve; and the Temminck's Seedeater (Sporophila falcirostris) at the Mbaracayú Forest Nature Reserve, Tapyta Private Nature Reserve, and Caazapá National Park.
The two Endangered species, the Black-fronted Piping-guan (Pipile jacutinga) and the Vinaceous-breasted Amazon (Amazona vinacea) have been recorded in 9 and 12 protected areas, respectively. The Purple-winged Ground-dove (Claravis geoffroyi), a Critically Endangered species, has only been recorded at Itabó Biological Reserve. Table 6. The UPAF endemic species with global conservation issues [14] and the number of core areas at the Paraguay Biodiversity Corridor with records of the species.

Birds with National Conservation Issues
A total of 120 bird species are included in lists of threatened and endangered species at a national level in Paraguay [37,38]. In the Paraguay Biodiversity Corridor, 91% (109) of these species have been recorded, of which 59 are threatened with extinction and 50 are endangered with extinction (Table 3). Table 7. The UPAF endemic species with national conservation issues [37,38], and the number of core areas within the Paraguay Biodiversity Corridor with records of the species.

Migratory Species at the Paraguay Biodiversity Corridor
Of the 557 bird species registered at the Corridor, 457 are confirmed residents breeding in the country. The 17.4% (97) are migrant species with different seasonal movements, and three species have no definite occurrence status because of deficient data [15].
Nineteen species are neartic migrants that breed in North America and migrate to the South of South America during the boreal winter. Forty-one species are northern austral migrants that breed in Paraguay and migrate to the North of South America in the austral fall and winter, when they are less abundant or absent.
Ten species are breeding southern austral migrants which breed in Paraguay but are more abundant in the austral winter with the arrival of more individuals from the south of South America.
Nineteen species are austral visitors, which pass by the country in the winter but do not breed here. Eight species are vagrant, with no clear pattern of occurrence in the country, being specially species with few records.

Bird Richness at the Paraguay Biodiversity Corridor
The total richness of 557 bird species recorded at the Paraguay Biodiversity Corridor of the UPAF represents more than 80% of the birds known for the country [15]. The richness of this Corridor, with an area of 12,000 km 2 , is higher than other ecoregions of globally concerned hotspots [2]. For example, most of the bird richness of the ecoregions of the tropical moist broadleaf forest biome of Mesoamerica ranges from 294 to 600 bird species, being the only one that surpasses the UPAF corridor, the Chocó/Darién moist forest. With a total of 600 bird species, the Chocó/Darien moist forest has an area of 10,294 km 2 and more than 50% is officially designated as protected areas [39]. Compared to other Atlantic Forest region, bird richness of the Paraguay Biodiversity Corridor is 17% higher than the Tibagi River Basin with an area of 24,530 km 2 , in the Paraná State of Brazil, with only 476 bird species recorded [40].
The Tibagi area which is two times bigger than the Paraguay Biodiversity Corridor is also a part of the UPAF ecoregion. This shows the high richness in the study area.
As mentioned before, core areas represent only 24% of the total area of the UPAF Corridor and only 3.5% of the original cover of the UPAF in the country. Some protected areas are Sustainable Management Resources Reserves (239 km 2 ), where 50% of the surface of the reserve are allowed to be managed for economic benefits, including agriculture, shade-grown plantations, or harvesting timber or non-timber products in the forest. While comparing the bird community in a shade-grown yerba mate plantation with the forest in one of the core areas, Itabó Biological Reserve, only 66% of the species of the forest were present in the plantation, being the understory, forest floor, and mid-story species more restricted to the forest; 40% of the species that were present in both habitats were two times more abundant at the forest, and five of the seven threatened species found in the forest were present at the plantation [41]. These results suggest that this sustainable activity does have lower impact in the forest bird community than traditional plantations and could be beneficial if used to rehabilitate some of the deforested areas, including areas where yerba mate is grown in the open [41]. The effects of selective logging on the bird community is still not evaluated at the UPAF in Paraguay, being one of the objectives of the censuses developed in this study. In the UPAF of Brazil, avian species richness and diversity were similar between a primary forest and logged forest; but species composition differed strongly, with understory and terrestrial insectivores as the most sensitive ecological groups [42].
Others core areas are partially protected (1004 km 2 ; Table 1). At the time of this study, only 12 protected areas were under strict protection, with a total of 127,818 hectares (10% of UPAF Corridor). The private sector contributes to the main surface of protected areas, with a total of 69,994 hectares, of which is mostly the Mbaracayú Forest Nature Reserve (65,134 hectares). Similarly, ITAIPU Binacional also provides most of strictly protected areas, with 40,655 hectares.
Seven private nature reserves have developed sustainable production of different resources of the forest; for example, the Itabo Biological Reserve extracts palm heart and produces shade-grown yerba mate; the Pindó, shade-grown yerba mate; the Ypetí, selective logging. These areas total 98,965 hectares of the Corridor. The effects of these human activities on the biodiversity of the forest are still not well understood.
The San Rafael National Park and the Mbaracayú Forest Nature Reserve are the core areas that hold higher richness of birds, with 427 and 408 species, respectively. This richness is also similar or higher than other protected areas in the Atlantic Forest in Brazil and Argentina, some of them being more than 30 times bigger than these two core areas of the Paraguay Biodiversity Corridor. In Brazil, the Iguaçu National Park, an area of 1850 km 2 , only has 335 species recorded [43,44] even though it is estimated that fewer than 400 species are found in the Park [43]. In the area of Saibadela of the Intervales State Park (380 km 2 ), in the southeast of Brazil, 234 species were recorded during an intensive study and 355 species were considered to occur at the area [45]. At the Sooretama Biological Reserve (240 km 2 ) in the Espíritu Santo State, 286 species were reported and at the Itatiaia National Park (300 km 2 ) in the States of Río de Janeiro and Minas Gerais, 251 species were found [46]. In Santa Catarina Island (425 km 2 ) in the Santa Catarina State, 269 species were known to have occurred in its area [47]. San Rafael and Mbaracayú surpasses all these sites in terms of total species richness.

Recommendations for the Management of Paraguay Biodiversity Corridor
The state of fragmentation and deterioration of the core areas of the Corridor require urgent actions so that biodiversity and natural resources can be preserved for the long term. Here are some of the key recommendations: (b) Legal enforcement: The San Rafael National Park is one of the areas with an ineffective protection, due to a lack of legal definition since its creation in 1992, as most of the area remains under private properties. More details about the situation of San Rafael have been detailed in 2007 [16], and it continues without any progress after 12 years. (c) Strengthening of authorities: Since 2004, a "Zero Deforestation" law have been applied to all the Oriental region of Paraguay. Regardless of the law, 6000 km 2 of the UPAF were deforested between 2003-2013 [6]. These illegal conversions of forest occur as there is a lack of control and punishment for these crimes. The authorities do not have the capacity nor an interest to work efficiently to impose this banning. An example that reflects the weakness of the authorities is that only 10 among 30 public Protected Areas managed by the state has an administration or a park ranger house, and there are only 64 park rangers employed to manage these areas, a number that is clearly insufficient for effective conservation purposes. (d) Research: The different types of pressure that effects the biodiversity of the UPAF are still not measured. Some of the main focus of research could be: Densities of endemic birds in the remnants of the UPAF; evaluating the impact of human activities such as selective logging on the bird communities of core areas (Agropeco, Ypeti and Tapyta Private Nature Reserve); and the impact of agriculture pesticides on the bird communities of remnants. Species accumulation curves showed that sample efforts for some of the grouped core areas (Kanguery, Itaipu) were insufficient to estimate species richness, especially when focusing on the Atlantic forest endemic. A higher sampling effort is required to improve comparisons of the bird richness of the UPAF core areas.

Conclusions
These results have demonstrated that the Paraguay Biodiversity Corridor contains a high bird species richness with a total of 557 species recorded at its core conservation areas. This richness surpasses sites with bigger areas in the ecoregion of neighboring countries. It has core conservation areas with high species richness, with the highest richness found in the San Rafael National Park (427 species), the Mbaracayú Forest Nature Reserve (408 species), the Tapyta Private Nature Reserve (377 species) and the Ypeti Nature Reserve (350 species). The Corridor also harbors 78 endemic bird species of the Atlantic Forest that occur in the country and 50 species of globally concerned conservation importance.
However, it is denoted that the main conservation core areas at the Corridor are fragmented and isolated, where the main landscape are cultivated lands and urban areas, covering over 50% of the surface. Likewise, only 24% of the Corridor area is included in a category of protected or sustainable management area, with only 10% under strict protection. The situation of the protected areas is alarming, considering that only 59% of the core conservation areas have a management plan, with protected areas like San Rafael not strictly protected, as it should be according to the category of protection designated by the government to this important bird area.  Acknowledgments: Dedicated to Salvador Peris, being his support and knowledge a major column of this work. Thanks to two anonymous reviewers and English edition by Tsewing Nuru Sherpa, an early draft of the manuscript was much improved.