Conservation of vulnerable Cerrado birds in an imminently threatened single large reserve

doi:10.21203/rs.3.rs-4907889/v1

The establishment of protected areas (PAs) is critical for mitigating anthropogenic impacts on biodiversity and maintaining ecosystem functionality. This scenario is more critical in extensively fragmented hotspots such as the Brazilian Cerrado. Therefore, addressing gaps in species composition, vulnerability, and abundance across different zoning interfaces, as well as potential threats to large reserves, are key steps in designing conservation actions. Here we evaluate abundance patterns and use of 17 vulnerable Cerrado birds across ecological zones, particularly Cerrado Stricto sensu and Riparian Forests in Chapada das Mesas National Park (NP). We demonstrate a positive scenario in terms of zoning effectiveness and bird conservation. Notably, the most vulnerable species in the NP are concentrated in areas of higher human occupation and tourist visitation, as well as along restricted-use territories. We also note that Cerrado stricto sensu subtypes constitute a single functional mosaic for endemic birds. Finally, we show that the NP may be imminently threatened by historical fires and potential future destruction of its adjacent ecosystems. Policies and actions focused on reducing deforestation and restoring habitats may represent the only way to prevent this single large reserve from becoming a major extinction site in the future.

Conservation

SLOSS

Territory

Connectivity

Ecological Zones

Avifauna

The global challenges aimed at restoring ecosystems, expanding protected area coverage, reducing extinction rates, and mitigating climate change effects are at the center of recent conservation discussions (Marzluff and Ewing 2001; Brancalion et al. 2019; Cazalis et al. 2020; Ceballos et al. 2020; Strassburg et al. 2020; Abhilash 2021; Carroll et al. 2023). Broadly speaking, establishing minimum dynamic areas and maintaining ecosystem heterogeneity are part of the globally proposed challenging solutions (Margules and Pressey 2000; Myers et al. 2000; Chetkiewicz et al. 2006). The effectiveness of such actions particularly demands information on species composition and abundance across habitat interfaces. In Single Large reserves within highly threatened hotspots such as the Cerrado, these gaps are even more concerning, especially given the current scenario of extensive ecosystem suppression in response to the expansion of monocultures, pastures, and large-scale developments.

Theoretical advances such as those discussing the SLOSS (Single Large or Several Small) scenario and the role of minimum dynamic areas for conservation are key elements in the current context of terrestrial ecosystem suppression and biodiversity loss (Novacek Cleland, E. E 2001; Ceballos et al. 2020; Riva and Fahrig 2022). The SLOSS debate gains greater relevance when considering Protected Areas that potentially constitute the main biodiversity refuges in the future but have had their adjacent ecosystems impacted (Hansen and DeFries 2007; Belote and Wilson 2020; Riva and Fahrig 2022). In this sense, projections warn that this may be the inevitable scenario for the Cerrado if urgent actions to combat deforestation, restoration, and spatial prioritization are not implemented (DeFries et al. 2007; Carvalho et al. 2009; Belote and Wilson 2020; Fahrig 2020; Riva and Fahrig 2022).

The Cerrado is one of the world's largest tropical savannas, home to approximately 980 bird species, of which 3.4% are endemic and 5% are threatened (Silva 1995; Carvalho et al. 2009; Aguiar et al. 2015; Françoso et al. 2015; Rodrigues et al. 2022). (Silva 1995; Myers et al. 2004; Silva and Santos 2005; Braz and Hass 2014; de Jesus et al. 2018; Colli et al. 2020; Braz et al. 2023). This biome plays a crucial role in the dynamics of major river basins, preserved especially by wet fields, palm swamps, floodplains, and extensive riparian forests (Aguiar et al. 2015; Colli et al. 2020). Despite its importance, the Cerrado has low protected area coverage (8.3%), which contrasts with the historical scenario of destruction of its territory. For example, between 1981 and 2012, about 300,000 hectares of land legally designated for protected areas were converted to monocultures (Carvalho et al. 2009; Aguiar et al. 2015; Rodrigues et al. 2022).(Carvalho et al. 2009; Borges et al. 2019; Colli et al. 2020). At current deforestation rates, up to 60% of the Cerrado's native vegetation could be destroyed by 2038 (Schwaida et al. 2023). Half of the biome's primary cover has already been replaced mainly by monocultures and pastures, which may result in the extinction of numerous species, especially birds (Colli et al. 2020; Rodrigues et al. 2022).

Birds represent the group with the highest number of species on the brink of extinction (n=335) compared to mammals (74), amphibians (65), and reptiles (41) (Ceballos et al. 2020; Lees et al. 2022). The historical decline in bird populations has resulted in a recent threat scenario where there may be fewer than 1,000 living individuals for each threatened species (Ceballos et al. 2020). Specifically, at least 1,213 bird species are threatened, and of this total, 13% are assessed as critically endangered (Lees et al. 2022). This panorama, which includes extensive destruction of terrestrial ecosystems, species decline, and imminent functional extinction, makes birds key organisms for conservation in ecosystems as vulnerable and threatened as the Cerrado (Sekercioglu et al. 2004; Şekercioḡlu 2006; Whelan et al. 2008, 2015; Buchanan et al. 2011; Wilson et al. 2016; Cazalis et al. 2020; Lees et al. 2022).

In threatened biomes such as the Cerrado and its avifauna, establishing protected areas with territories designated for different purposes becomes crucial, especially in single large reserves. Ecological zoning aims to set boundaries and direct activities in specific territories within protected areas based on the multiple habitats that compose their landscapes (Rotich 2012; Herrera-Montes 2018; IUCN 2024). Zones reflect the intended land use established in the management plan, the expected level of anthropogenic impact, and existing use patterns in these areas (Dudley and Stolton 2008; Herrera-Montes 2018). Thus, zoning represents selective control of activities in different locations, concentrating high, intermediate, and low-degree anthropogenic impacts in specific zones (Rotich 2012). Actions specifically focused on conservation and management of natural resources, research, ecotourism and recreation, as well as visits to fossil sites or rock art, are highlighted (Herrera-Montes 2018). Particularly in large protected areas such as national parks, numerous gaps remain regarding the composition and vulnerability of avifauna, as well as patterns of abundance and use of different phytophysiognomies, and the vulnerability of these protected areas in the face of destruction of adjacent ecosystems.

Here we evaluate patterns of abundance and use of different ecological zones and phytophysiognomies in Chapada das Mesas National Park (NP) based on 17 vulnerable Cerrado birds. In addition, we present a vulnerability scenario of the NP based on fires and annual deforestation rates, demonstrating the persistence of these disturbances as well as the potential extinction of ecosystems adjacent to the NP.

Study area

The study was carried out in the Chapada das Mesas National Park (NP), located in the south-central region of the state of Maranhão, Brazil (-7.168S and -47.150W), (Fig. 1, a-b), from August 2021 to December 2022. This period covered the dry winter (May to October) and the rainy summer (November to April), (Ab’Saber 1977; ICMBio 2019). Covering the municipalities of Carolina, Estreito and Riachão, the NP has 160,046 thousand hectares with phytophysiognomies ranging from dense cerrado, sparse cerrado, typical cerrado, cerradão, clean field and extensive riparian forests (ICMBio 2019). The NP is also an important ecotone, with physiognomic elements from the Cerrado, the Amazon and the Caatinga. The tropical climate predominates in the region and is marked by high temperatures throughout the year, with an annual average of 25.1°C to 26.1°C and rainfall estimated at between 1,250mm and 1,500mm (ICMBio, 2019).

In detail, the NP (Fig. 1, b) is divided into three zones according to its management plan, two of which are intended for visitation and one exclusively for conservation. They are: 1) Moderate Use Zone (MZ) - with a semi-intensive impact; 2) Infrastructure Zone (IZ) - with an intensive impact and 3) Conservation Zone (CZ) - with a low level of anthropogenic impact. The first (MZ) is the largest zone in the NP with 102,046 hectares (ha) subdivided into four polygons comprising natural or moderately anthropized environments of medium and advanced degree of regeneration (ICMbio, 2019). Activities such as research, protection, recovery, environmental monitoring, visitation of a medium degree of intervention and the construction of small buildings such as staircases for ecological trails or campsites are allowed within the area (ICMBio, 2019).

The infrastructure zone (IZ) occupies the second largest area in the NP (32,000 ha). In detail, the IZ constitutes the territory under the greatest human occupation, thus concentrating the impact of activities with a high degree of anthropic intervention, such as those associated with the infrastructure intended for visitation and the administration of the NP (ICMBio, 2019). Finally, the conservation zone (CZ) occupies the smallest area of the NP (26,000 ha), sheltering environments of relevant scientific, ecological and landscape interest with little anthropogenic intervention. Its priority objective consists of the continued management and preservation of natural areas in order to keep them as close to the original as possible, and to target research and visitation with a low degree of interference (ICMBio, 2019).

Data collection

The bird communities were recorded by means of an auditory and visual census using linear transects (Magnusson et al. 2005). We selected polygons representing the three zones in the NP where three transects (T) were established. In detail, these were T1 (-6.984S and -47.369W), in the Porão/Farinha MZ; T2 (-7.045S and -47.190W), in the Prata/São Romão IZ and T3 (-7.154S and -47.392W), in the Cancela CZ (Fig. 2). Each transect was 4 km long with a species detection area defined as 100m on the side (Fig. 2). These were divided into 500m routes which, in turn, made up the study's sampling unit. A new species list was produced at the start of each route. To ensure independence between the samples, the observer assessed the potential or actual displacement of individuals between one route and the next. Field sampling was carried out by a single observer (ESF) and the average distance between the three transects was 21.6km from the start. The sampling effort was established according to the representativeness of the zones in terms of extension in the NP (Table 1).

The transects selected covered four of the seven phytophysiognomies described in the NP (Fig. 2). The Cerrado stricto sensu was represented by the typical Cerrado (Cerrado woodland), Cerrado ralo (Open Cerrado) and Cerrado denso (Dense savanna woodland) and the Cerrado florestal was represented by the Floresta riparária and/or Mata Ciliar (Ribeiro and Walter 2008). Conventionally, we will use the term "Riparian forest" to specify the Forest Cerrado and "Cerrado stricto sensu" when we refer to the subtypes of savanna formations together.

Table 1. Sampling effort (top row) and study period.

MZ - (121 routes)	IZ - (56 routes)	CZ - (47 routes)
11-13 de October and 10-13 of November (2021).	20 of September, 14 of Oct. and 12 of Nov. (2021).	18 of Aug., 20 of Sep., and 15 of Oct. (2021).
15-16 of February and 4-6 of April; 22-24 of August and 13-14 of December (2022).	14 of Feb., 5 of April; 24 of Aug. and 15 of Dec. (2022).	15 of Feb., 4 of April; 23 of Aug. and 15 of Dec. (2022).

During each transect, the observer recorded data on species abundance and composition. Sampling took place systematically from dawn until around 10 a.m., when the species stopped vocalizing and moving around. To compensate for morning expeditions that were eventually prevented by rain, sampling was carried out between 2pm and 6pm, making up 7.1% of the total effort. The species' vocalizations were recorded using a digital recorder (Zoom H1 - Handy recorder), and the observations were made using Nikon Monarch 10x42 binoculars. The birds were identified using field guides (Perlo 2009; Ridgely & Tudor 2009; Sigrist 2010, 2013), digital voice banks and consultations with experts. In addition, global (IUCN 2023) and national (ICMBio 2018) lists of threatened species were consulted and key records were deposited on the Xeno-canto (Xenocanto 2023) and Wikiaves (Wikiaves 2023) platforms. The list of species evaluated followed the nomenclature guidelines defined by the Brazilian Committee of Ornithological Records (Pacheco et al. 2021).

Definition of target groups

After compiling the general list of species recorded in the field, we defined two target groups: (G1) species endemic to the Cerrado (Silva 1995; Sigrist 2010) and (G2) species of high ecological sensitivity (Parker et al. 1996; Stotz et al. 1996) or included in the National Action Plan for the Conservation of Birds of the Cerrado and Pantanal (PAN Cerrado-Pantanal), (Brasil 2023), excluding endemic species from this criterion. Based on this definition, birds will be referred to generically here as "G1 species" or "G2 species" and as "vulnerable species" when mentioned together.

Essentially, endemic species are critical in the development of strategies to prevent extinctions at a national and global level, especially due to their ecological particularities in terms of habitat use and vulnerability (Kraus et al. 2023). The species of high ecological sensitivity and those included in the PAN Aves do Cerrado e Pantanal are thus grouped based on their degree of threat and priority in conservation and research. In addition, ecological aspects such as foraging stratum, type of habitat or micro-habitat and density patterns in space define them as vulnerable species (Parker et al. 1996; Stotz et al. 1996; Brasil 2023).

Statistical analysis

To assess the abundance patterns of G1 and G2 species across zones and phytophysiognomies, we carried out Analyses of Variance (ANOVAs), (p<0.05), (Sawyer 2009). In the ANOVAs we used the Welch correction to estimate (Ahad and Yahaya 2014), since there were no homogeneous variances. In addition, we used the Monte Carlo algorithm with 9999 randomizations to estimate the p-value (Koch 2018). When there was a difference, we used the Tukey a posteriori test (Salkind 2012) to graphically indicate which zones and phytophysiognomies are different in abundance.

In order to analyze whether the species form specific groups or are widely distributed throughout the zones and their respective phytophysiognomies, we carried out Principal Component Analyses (PCAs), (Jollife and Cadima 2016), one for each target group of species based on the abundance data. Each species represented a variable and each zone and phytophysiognomy a locality in the PCAs. In addition, we carried out ANOVAs to assess whether there was a significant difference between the orderings, treating the scores of the principal components as a simple univariate variable (Nicholas J. Gotelli and Ellison 2010). The criteria for evaluating the ANOVAs and a posteriori analyses were the same as those described above.

Vulnerability analysis of the NP

In order to provide an overview of the NP's vulnerability to historical disturbances, we obtained shapes of deforestation and annual fires that occurred in and around the NP between 2000 and 2022 (MapBiomas 2023). The shapes for the surrounding area included the municipalities of Carolina, Estreito, Riachão and Feira Nova do Maranhão (MapBiomas 2023).

Subsequently, we extracted the values for the annual rates of these impacts from the deforestation shapes (MapBiomas 2023) and built time series projections for the following 28 years, starting in 2022. The aim was to assess historical and future patterns of suppression in and around the NP. During this process, we did not consider the overlaps between the boundaries of the NP and the municipalities to ensure that the data from inside and around the NP were analyzed independently. We thus sought to assess whether, based on historical patterns, there is a prospect of a reduction, increase or persistence of deforestation in the interior and surroundings of the NP. We used the Smoothing forecasting technique and the Linear trend function (SINGH et al., 2019) to assess deforestation patterns in the specified municipalities and in the NP.

This vulnerability perspective is based on the assumption that the suppression of adjacent ecosystems directly impacts biodiversity within PAs. This is due to the potential extinction or reduction of external sources of colonizers and, therefore, changes in the colonization-extinction dynamic between the PA and its surroundings (DeFries et al. 2007; Laurance 2008; Wilson 2009; Fahrig et al. 2022; Szangolies et al. 2022). In this way, populations become more vulnerable to demographic and environmental stochastic events, and therefore susceptible to extinction events even within PAs (Lahti and Ranta 1985; DeFries et al. 2007; Laurance 2008; Takashina 2021; Fahrig et al. 2022; Szangolies et al. 2022; Rutt et al. 2023).The analyses and graphs were built using Past (v. 4.03) and Statistica (v.10), (Statsoft 1999). The maps were made using the test version of the Arcgis program (Esri 2023).

We recorded 17 species that made up the target groups, including three near-threatened birds (NT) and one threatened bird (VU) based on global and national criteria (Table 2). In a global scenario, we found that the infrastructure zone (IZ) and the moderate use zone (MZ) had the highest abundances of G1 species, and were statistically equal in this respect (Fig. 3, a). The conservation zone (CZ), on the other hand, had the lowest abundances of this group of species (F= 21.63; df= 11, 83; p= 0.0024) (Fig. 3, a). When we evaluated the G2 species, we found that they showed equal abundances between the different zones (F= 1.52; df= 24.71; p= 0.21), (Fig. 3, b). Additionally, we noticed that the G1 species are particularly concentrated in the IZ and MZ, forming a distinct group from those located in the conservation zone (F= 13.75; df= 11.33; p= 0.00699 - PC 1), (Fig. 4, a).

Table 2 - Target groups and their conservation status. - = bird not included in the Red List of Threatened Species (Brazil 2022) or in the PAN of Birds of the Cerrado and Pantanal (Brazil 2023).

Species	English Name	IUCN	ICMBio	Group
Cercomacra ferdinandi	Bananal Antbird	NT	VU	G1
Charitospiza eucosma	Coalcrest	NT	-	G1
Cyanocorax cristatellus	Curl-crested Jay	LC	-	G1
Cypsnagra hirundinacea	White-rumped Tanager	LC	-	G1
Melanopareia torquata	Collared Crescentchest	LC	-	G1
Neothraupis fasciata	White-banded Tanager	NT	-	G1
Saltatricula atricollis	Black-throated Saltator	LC	-	G1
Ara chloropterus	Red-and-green Macaw	LC	-	G2
Campephilus rubricollis	Red-necked Woodpecker	LC	-	G2
Campylorhamphus trochilirostris	Red-billed Scythebill	LC	-	G2
Dromococcyx pavoninus	Pavonine Cuckoo	LC	-	G2
Habia rubica	Red-crowned Ant-tanager	LC	-	G2
Patagioenas subvinacea	Ruddy Pigeon	LC	-	G2
Procnias averano	Bearded Bellbird	LC	-	G2
Ramphastos vitellinus	Channel-billed Toucan	LC	-	G2
Ibycter americanus	Red-throated Caracara	LC	-	G2
Amazona aestiva	Turquoise-fronted Amazon	NT	NT	G2

The species with the greatest weight in explaining this pattern of use of the zones were Melanopareia torquata, Cyanocorax cristatelus and Charitospiza eucosma (Fig. 4, b). From a second perspective, the G1 species were widely distributed throughout the three zones and did not form distinct groups in terms of their use of these territories (F= 1.03; df= 11.61; p= 0.21 - PC 2). In this scenario, Cyanocorax cristatelus stood out as the species that most contributed to this picture of the use of multiple zones (Fig. 4, c). When evaluating the G2 species they also showed a wide distribution throughout the three zones evaluated (Fig. 5, a). In particular, Procnias averano, Campylorhamphus trochilirostris e Ara chloropterus (F= 0,36; df= 25,77; p= 0,68) stood out as the species that most contributed in explaining this scenario (Fig. 5, b).

Table 3 - Eigenvalues and percentage of explanation of the axes generated from the evaluation of each target group via PCAs. Var. (%)= percentage of variance explained.

Axis	G1 Species		G2 Species
PC	Eigenvalues	Var. (%)	Eigenvalues	Var. (%)
1	27,38	50,69	21,35	53,29
2	16,80	31,10	7,27	18,15
3	4,01	7,43	5,46	13,63
4	2,71	5,02	4,28	10,68
5	1,78	3,29	0,77	1,92
6	1,18	2,18	0,45	1,13
7	0,15	0,27	0,24	0,59
8	-	-	0,12	0,30
9	-	-	0,10	0,26
10	-	-	0,02	0,06

In addition, when evaluating the patterns of vulnerable species along the phytophysiognomies covered by the transects, we found that the typical Cerrado had higher abundances of G1 (F= 21.63; DF= 11, 83; p= 0.0024) and G2 (F= 8.69; DF= 13.05; p= 0.0067) species than the Riparian Forests (Fig. 6, items 1-2). As a result of the same analysis, the typical Cerrado showed the same abundances of vulnerable species when compared to the dense Cerrado, sparse Cerrado and Riparian Forests (Fig. 6, 1-2). When evaluating the use patterns of the phytophysiognomies, we first noticed that the G1 species occur in two distinct groups of formations. In detail, the Cerrado stricto sensu constitutes a single mosaic for these species which, in turn, form distinct use groups from the Riparian Forests (F= 5.07; DF= 33.04; p= 0.0100), (Fig. 7, item 1). The G1 species with the greatest weight in explaining these patterns were Melanopareia torquata, Charitospiza eucosma, and Cyanocorax cristatelus, respectively (Fig. 7, 2).

On the other hand, we found that the G2 species are distributed across all four phytophysiognomies and do not form distinct groups in terms of their use of these formations (F= 3.44; DF= 13; p= 0.06) (Fig. 8, 1). Thus, the Cerrado stricto sensu and Riparian Forests represent a single functional mosaic for the G2 species. This demonstrates the spatial patterns of connectivity and, therefore, transition of vulnerable species along the savannah and forest formations (Ribeiro and Walter 2008) along the different zones in the NP. The G2 species with the greatest weight in determining these patterns of use of the phytophysiognomies were Procnias averano, Campylorhamphus trochilirostris and Ara chloropterus, respectively (Fig. 8, 2).

By overlaying the annual fire data, we show that these disturbances are prevalent both inside and around the NP (Fig. 9), in addition to the alarming scenario of deforestation in adjacent ecosystems (Fig. 10). By projecting the time series based on historical deforestation data in the interior of the NP, we show a historical downward trend and the future prospect of no loss of native vegetation for at least 25 years from 2025 (Fig. 11, item a). Although we have noticed a historical and future reduction in deforestation around the NP, we would warn against two worrying scenarios. Firstly, there have been regular historical periods of deforestation (2000-22) above 2,500km² per year (Fig. 11, b). When we project this scenario to the following 28 years (2022-50), we note that these rates will potentially remain at least around 1,500km²/year (Fig. 11, b), which would have an extensive impact on the ecosystems adjacent to the NP.

In the general context where we evaluated abundance patterns between zones, we showed that the infrastructure zone (IZ) and moderate use zone (MZ) concentrate the highest abundances of endemic birds. In addition, we noted that endemic species are distributed particularly in the IZ and MZ and that, from another perspective, these species occur widely in the conservation zone (CZ), IZ and MZ. Under a general approach to the use of phytophysiognomies along the transects, we analyzed the abundance patterns of vulnerable birds along the Cerrado stricto sensu and Riparian Forests in the NP. We also assessed how the species are distributed across these phytophysiognomies and presented a scenario of historical and future vulnerability of the NP based on annual fires and deforestation in and around the area.

Patterns and key species for conservation in the NP

The prevalence of endemic birds in the NP may be due to the wide coverage of native vegetation and, therefore, the low impact of anthropogenic activities on Cerrado stricto sensu formations and Riparian Forests in the three zones, especially IZ and MZ (Aguiar et al. 2015; Schwaida et al. 2023). These zones were originally intended for visitation in the NP, covering 83% of its extension (ICMBio 2019),, and have proved crucial for the conservation of the vulnerable birds assessed here. In more detail, the Cerrado stricto sensu and Riparian Forests, in turn, occupy the majority of the NP (92%), (ICMBio 2019). However, we reiterate the need for future studies on the composition, richness and diversity of birds in phytophysiognomies not assessed here. In this sense, the Campo Limpido Humidum/Vereda (2.9% of the PA), Campo Limpido/Sujo (2.1%) and Cerradão (0.5%) are formations that potentially harbor critical habitats, including potential Cerrado endemics in the NP.

In this way, we emphasize that this scenario is extremely positive, since the persistence of endemic birds in these territories may be a reflection of the proper design of management actions and use of the territories. Therefore, we stress that maintaining minimum viable populations of vulnerable birds by conserving the heterogeneity and coverage of native vegetation in these locations may be perfectly feasible. For this reason, our study reinforces the need to reconcile sustainable management practices and ecotourism in the search for greater conservation effectiveness in the NP and in reserves with similar zoning contexts (Stronza et al. 2019; Develey 2021; Lees et al. 2022). This perspective is corroborated especially because the transect evaluated in IZ is part of one of the access routes to the second main tourist attraction in the NP. It is estimated that the Cachoeira da Prata (-6.99S and -47.165W) receives around 10,000 to 12,000 tourists a year (REGO, 2023 - head of the NP; Personal communication), a visitation dynamic that apparently has had no impact on the persistence of vulnerable birds in IZ (ICMBio 2019).

From a broader point of view, we stress that the planning of actions for the conservation and management of the NP, and particularly of its avifauna, should consider two fronts (Margules and Pressey 2000). Therefore, long-term systematic monitoring of bird communities (1), (De Lima et al. 2022; Pollock et al. 2022) and the inclusion of local residents in actions to combat natural and anthropogenic impacts (2) are key actions (Dawson et al. 2021). This is especially relevant given the essential role of large PAs in the conservation of the Brazilian Cerrado and the crucial need for continued action in this direction (Dawson et al. 2021; Pollock et al. 2022).

Of the seven endemic birds evaluated here, six have been recorded in an IBA in the state of Maranhão: Neothraupis fasciata (Chapada dos Veadeiros National Park), Melanopareia torquata, Cypsinagra hirundinacea, Cyanocorax cristatellus, Charitospiza eucosma and Saltatricula atricollis (Boa Esperança Dam), (De Luca et al. 2009). In specific terms, we would point out that the wide distribution of M. torquata, C. cristatellus, and C. eucosma, Procnias averano, Campylorhamphus trochilirostris, and Ara chloropterus throughout the three zones and phytophysiognomies may be a reflection of the dynamic connectivity between the savannah and forest formations in the NP. For example, M. torquata is a bird typical of grassland regions predominantly made up of sparse Cerrado, especially landscapes rich in termite mounds and insects (Sick 1997; Sigrist 2010). On the other hand, C. cristatellus is a typically arboreal species that occupies transition zones encompassing grassland and densely wooded areas, and is not restricted to a single habitat (Sick 1997; Sigrist 2010). With a similarly dynamic ecological preference, Charitospiza eucosma usually uses both spaced shrubs and Cerrado fields (Sick 1997; Sigrist 2010).

More specifically, P. averano is among the most important dispersers of plants through the consumption of fruits that make up its typically frugivorous diet (Sick 1997). The species has been included among the endemic and threatened birds of crucial importance in the conservation of the Atlantic Forest in northeastern Brazil, especially due to its presence in ecotonal regions (Pereira et al. 2016). This reiterates the potential role of Procnias averano as a target species for the conservation of vulnerable birds in the NP, especially since this PA is made up of multiple phytophysiognomies and ecotonal interfaces. Similarly, the wide occurrence of C. trochilirostris throughout the three zones may be a direct reflection of the connectivity between these territories. This hypothesis is reinforced since the species is typically associated with flooded riparian forests, potentially transiting along these formations that connect a range of phytophysiognomic formations in the NP (Sick 1997; Bennett 2003a, b; Sigrist 2010; ICMBio 2019). Furthermore, C. trochilirostris is perhaps the species that clearly represents the dynamics and distribution of the more than 400 springs of the Tocantins River present in the NP (ICMBio 2019). This is why we emphasize that the numerous riparian corridors and, consequently, the diversity of habitats present in the different zones are critical aspects in terms of the connectivity and conservation of the NP (Sick 1997; Beier and Noss 1998; Bennett 2003a; Wiegand et al. 2005; Sigrist 2010; ICMBio 2019; Fischer et al. 2021; Pörtner et al. 2021). Although assessed as a species not at risk (LC), Ara chloropterus is a bird that, similar to the others mentioned above, moves between savannah and forest formations (Sick 1997; Sigrist 2010). This reinforces the patterns shown here in which the vulnerable birds of the NP are widely distributed throughout the zones and particularly concentrated in the Cerrado Stricto Sensu and Riparian Forest formations.

In terms of vulnerability, A. chloropterus is one of the main targets of wildlife trafficking in Brazil (Halle 2018). For example, almost 30,000 specimens were exported to more than 55 different countries/territories between 2000 and 2013 (Halle 2018). The impact of population decline resulting from habitat loss and trafficking are such imminent risks to the species that it has been considered virtually extinct in Rio de Janeiro, vulnerable in Paraná, and critically endangered in São Paulo (Halle 2018; WWF 2021).

In a similar context, the true parrot (Amazona aestiva) is one of the psittaciformes most threatened by wildlife trafficking in Brazil and South America (Costa et al. 2018; Halle 2018). The search for specimens of A. aestiva is fueled especially by its extraordinary ability to imitate, which is why it is considered the most "talkative" species and one of the rarest parrots, from this illegal perspective (Sick 1997; Sigrist 2010; Halle 2018). In just 13 years, A. aestiva has had 60,780 individuals exported outside South America. In particular, South Africa and Argentina accounted for almost 80% of this illegal export (Halle 2018). In addition, we would highlight the fact that the species is among the main taxa received at Wild Animal Rehabilitation Centers (CETAS). This has occurred mainly because A. aestiva is the target of clandestine capture after the reproductive period, when the chicks are under parental care (Costa et al. 2018; Halle 2018). Particularly in Brazil, between 2005 and 2009, CETAS received 250,206 birds which, in turn, corresponded to the biological group with the highest number of individuals killed due to mistreatment in captivity (86%), (Destro et al. 2012). In the same period, A. estiva was the 15th most seized bird in enforcement and anti-trafficking operations (Destro et al. 2012). In this sense, given the intense flow of tourists that predominates in the NP, we cannot rule out the hypothesis that A. aestiva may attract criminal actions aimed at capturing it and other birds of economic interest. This scenario reinforces the importance of periodic inspections in large PAs which, similar to the NP, are home to psittaciformes as vulnerable and targeted by trafficking as A. chloropterus and A. aestiva.

From a final perspective of analysis in terms of ecology and vulnerability, C. ferdinandi is a species whose way of life (OLMOS; SILVA; PACHECO, 2006) clearly reflects the dynamics of connectivity and transition between the Cerrado Stricto Sensu and forest landscapes (Ribeiro and Walter 2008). The species tends to forage near bodies of water and occurs along riparian or gallery forests, preferably in dense lianas and shrubs (Sick 1997; Sigrist 2010, 2013). In addition to this availability of habitat, the choice of climatic biodiversity refuges with a focus on species as vulnerable as C. ferdinandi is a fundamental strategy in Cerrado conservation planning (Borges et al. 2019; Borges and Loyola 2020). This is because the species is among the four birds that will potentially be most vulnerable in the Cerrado in 27 years (Borges and Loyola 2020). The reason is that its occurrence could be restricted to areas completely outside those indicated as refuges in the face of the synergistic impact of deforestation and climate change (Borges et al. 2019; Borges and Loyola 2020). In detail, Cercomacra ferdinandi, along with Pyrrhura pfrimeri, Synallaxis simoni, and Paroaria baeri, has conservation priority, essentially with a focus on monitoring their populations (Borges and Loyola 2020). Fortunately, in the interior of the NP, the forecasts are positive in terms of deforestation (Fig. 7, 1), however, we warn of the long-term destructive effect that fires can have on the habitats critical to the population maintenance of C. ferdinandi. Until recently, the species was recorded predominantly in PAs located in the state of Tocantins (Cantão State Park, Araguaia National Park, Bananal Island Environmental Protection Area), (Dornas and Pinheiro 2018). Therefore, recording the species in the NP broadens the prospects in terms of conservation, especially with a view to mapping key areas for establishing ecological corridors that include the species' distribution and living areas (Olmos et al. 2006; Sigrist 2010; Dornas and Pinheiro 2018; Ferreira 2021).

Taken together, projections indicate that the occurrence of these species will be limited to regions with a greater extent of native vegetation, however, under high climatic abnormalities (Borges and Loyola 2020). In this sense, we are alerted to the fact that the NP is located in one of the regions where there will potentially be less native Cerrado vegetation cover and climate instability by 2050 (Borges and Loyola 2020). This reinforces the primary role of the NP in the conservation of C. ferdinandi, since this PA is still home to an area mostly made up of primary Cerrado formations and their ecotonal transitions (97.7% coverage), (ICMBio 2019). In addition, the NP is at the limit of C. ferdinandi 's distribution, which potentially includes key microhabitats for the conservation of the species both within the PA and along adjacent ecosystems. Since C. ferdinandi was only recorded once in this study, we would like to point out that there are still numerous gaps, notably knowledge regarding reproductive sites, density patterns and the species' home range in the NP. Among the priority actions for the conservation of C. ferdinandi is the mapping of relevant areas for the implementation of ecological corridors throughout its area of occurrence (Olmos et al. 2004; Pinheiro and Dornas 2009; Dornas and Pinheiro 2018). This makes the NP and its multiple networks of riparian corridors and springs a potential scenario for the conservation of the species. Especially, the expansion of dams and hydroelectric plants on the Tocantins River, particularly the Estreito Hydroelectric Plant (Maranhão), represent the main threats to populations of C. ferdinandi (Olmos et al. 2004; Pinheiro and Dornas 2009; Dornas et al. 2012).

This reinforces the need to expand our knowledge of the species' biology and distribution in the NP, where its populations are theoretically protected from these threats. More broadly, this myriad of available habitats are potential targets for practices such as multi-species monitoring via radiotelemetry, the release of post-rehabilitation individuals in CETAS or the strengthening of endangered species via reintroduction or translocation. Therefore, systematic long-term planning becomes critical in the NP, especially considering the current and future picture of destruction in the Cerrado and increased susceptibility to fires in response to climate change. The potential effect of stressors on the NP's avifauna due to the influx of tourists and the vulnerability of species to wildlife trafficking also reinforce this picture of threats. We therefore highlight the unique importance that the NP represents for the conservation of the Cerrado, its vulnerable species and biodiversity expressed through provisioning services, regulation, cultural values and well-being.

The potential future vulnerability of the NP as a Single Large reserve

The NP is at an average distance of 180 km from other PAs which, in detail, are the Mata Grande Extractive Reserve and the Parnaíba River Springs National Park (Maranhão) and the Tocantins Fossilized Trees Natural Monument. This makes the NP a Single Large reserve immersed in an unprotected matrix and under historic anthropogenic impacts.

Large PAs such as the NP constitute effective barriers against deforestation in the Cerrado (Nelson and Chomitz 2009). As we have shown here, deforestation has shown a historical reduction under a future perspective of annual rates that could reach zero from 2025 onwards (Fig. 7, 1). However, we also note that the ecosystems adjacent to the NP could be completely impacted by deforestation (Fig. 7, 1). This is critical given that the reduction in effective size as well as the loss of crucial habitats in response to anthropogenic impacts results in the destruction of external sources of colonizers (Lahti and Ranta 1985; DeFries et al. 2007; Belote and Wilson 2020; Fahrig et al. 2022; Riva and Fahrig 2022; Szangolies et al. 2022). In terms of bird conservation, adjacent ecosystems play an essential role. This is because populations can concentrate in small hotspots outside PAs, potentially harboring individuals of critical importance in species turnover (Brown 1984; Brown and Kodric-Brown 1997; Hanski 1998; Hanski and Ovaskainen 2000). From this perspective of prevalent fires in and around the interior and the extensive suppression of ecosystems adjacent to the NP, we warn that this PA could represent a major site of extinctions in the future (Simberloff and Abele 1976; Pickett and Thompson 1978; Fahrig 2020). More specifically, with low or zero colonization rates, extinction becomes the dominant process in populations, impacting the dynamic balance of the PA and culminating in the long-term decline of species (Pickett and Thompson 1978; Hansen and DeFries 2007).

This context reinforces the urgency of making political decisions that substantially reduce deforestation in the area surrounding the NP. As it is a Single Large reserve, ecological restoration programs and the establishment of corridors that include adjacent ecosystems are key strategies for mitigating these potential impacts. Particularly in the Cerrado, the remnants of native vegetation adjacent to PAs have been mostly converted into monocultures and pastures (Carvalho et al. 2009; Aguiar et al. 2015; Françoso et al. 2015; Schwaida et al. 2023). This brings us to a challenging global scenario involving destructive land use and occupation models, the urgent need to restore ecosystems and establish dynamic areas (Several Small), (MMA 2010; Françoso et al. 2015; Edwards et al. 2019; Belote and Wilson 2020; Fahrig 2020; Riva and Fahrig 2022).

Theories such as metapopulation dynamics (Hanski 1998), island biogeography (Simberloff and Abele 1976; Wilson 2009) as well as disturbance ecology (Rykiel 1985; Burton et al. 2020) and landscape ecology (Hobbs 1993; Wiens 2009) have sought to understand the processes that determine spatial patterns in dynamic ecosystems such as those present in the NP (DeFries et al. 2007; Belote and Wilson 2020; Fahrig et al. 2022; Riva and Fahrig 2022; Szangolies et al. 2022). Overcoming this challenge requires understanding not only the patterns of internal dynamics between the mosaics of habitats and phytophysiognomies, but above all the role of adjacent ecosystems in maintaining biodiversity within PAs (Brown 1984; Hanski 1998; Belote and Wilson 2020). The imminent biotic homogenization in response to the extensive global destruction of natural remnants has resulted in a scenario of functional destabilization in ecosystems (Jongman 2002; Wang et al. 2021). Additionally, on a landscape scale, disturbance regimes determine the successional stages of communities along habitat patches, as well as their size and density (Pickett and Thompson 1978). Even knowing the adaptive potential of Cerrado species to fires (Simon and Pennington 2012), an imminent scenario of vulnerability may be unfolding. If we consider the current situation of deforestation around the NP, high temperatures, prolonged droughts and, therefore, greater susceptibility to fires, this PA could lose its resilience in the long term. (Carvalho et al. 2009; Françoso et al. 2015; Zalles et al. 2019; Borges and Loyola 2020; MapBiomas 2023). Therefore, this threat potentially represents one of the clear reflections of environmental stochastic dynamics and its long-term negative effects on PAs (Takashina 2021).

Current and future prospects for the conservation of the NP

The patterns of abundance and use of the zoning interfaces and phytophysiognomies from the birds assessed here constitute a key initial step for continued monitoring and conservation actions in the NP. In this sense, the NP and PAs, which similarly have extensive native vegetation cover, can be effective in conserving vulnerable Cerrado birds, even though they are mostly used for visitation and ecotourism. The myriad of habitats still conserved are key targets in terms of connectivity and conservation in the NP, and are potential targets for practices such as multi-species monitoring via radiotelemetry, release of individuals after rehabilitation in CETAS or population strengthening of threatened species via reintroduction or translocation. Therefore, systematic long-term planning becomes critical in the NP, especially considering the current and future picture of destruction in the Cerrado and increased susceptibility to fires in response to climate change. The potential effect of stressors on the PN's avifauna due to the influx of tourists and the vulnerability of species to wildlife trafficking also reinforce this picture of threats. In this sense, we emphasize the crucial role of the NP for the conservation of the Cerrado, its vulnerable species and biodiversity expressed through provisioning services, regulation, cultural values and well-being.

From a warning perspective that includes the internal dynamics of connectivity, susceptibility to fires and the potential future impact that the destruction of adjacent ecosystems could have on the NP, we highlight some alternatives. Actions to combat deforestation and fires of anthropogenic origin in and around the NP should be a priority. In addition, we suggest establishing restoration programs around the NP, taking into account unprotected natural areas, as well as expanding knowledge about the home range, distribution and reproductive sites of the species targeted in this study. In addition, we emphasize that the NP is a key territory for the conservation of vulnerable Cerrado birds, given the current scenario of species extinction, increased catastrophes in response to climate change and global efforts to restore terrestrial ecosystems. However, we warn of the NP's vulnerability to the imminent destruction of adjacent ecosystems. Substantially reducing deforestation and restoring these territories may be the only way to prevent this Single Large reserve from becoming a site of long-term extinctions.

Competing interests. The authors declare that there is no conflict of interest and that, particularly, the author Marcos Pérsio Dantas Santos is Associate Editor for Ornithology Research and the peer-review process for this article was independently handled by another member of the journal editorial board.

Funding Declaration

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001

Author Contribution declaration

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No competing interests reported.

Conservation of vulnerable Cerrado birds in an imminently threatened single large reserve

Status:

Version 1

Abstract

Figures

Introduction

Methods

Results

Discussion

Declarations

References

Additional Declarations

Status:

Version 1