Introduction

The Atlantic Forest ecoregion in southeast Brazil, eastern Paraguay, and northeastern Argentina, is one of the biogeographic regions with the highest diversity in the world [12–3]. However, it is now critically threatened by increased anthropogenic pressure, such as selective logging and agricultural expansion (the most important human activities in this region)[23–4]. This ecoregion includes the Upper Paraná Atlantic Forest, which originally covered an area of 81 million hectares in southern Brazil, eastern Paraguay, and northeastern Argentina (province of Misiones). At present, only 5% of the original forest remains intact, and the degree of forest conservation and fragmentation differs among countries. Brazil and Paraguay are critically affected, while 50% of the original area remains in Argentina [5, 6]. Nevertheless, this scenario is changing rapidly in the Argentine province of Misiones, where the Paranaense Forest (sensu Cabrera [7]) has undergone intense deforestation in recent decades [4, 2], fragmenting the landscape with forest patches in different degrees of alteration [2, 5, 8]. A major forest nucleus in the Atlantic Forest is formed by the connected protected areas of Iguaçu National Park in Brazil, Iguazú National Park, and Urugua-í Provincial Park in Argentina (Fig. 1). At the southeast of this nucleus an ecological corridor links Urugua-í Provincial Park to Horacio Foerster Provincial Park (hence forth ECU-F) (Fig. 1). This corridor was created to preserve or restore the connectivity between the provincial parks because the site is crossed by several roadways, bringing associated urbanization, deforestation, fragmentation and resource extraction [6]. The goal of ECU-F is to restore the structure and functioning of native humid forests in areas that were converted to pasture or cropland and then abandoned, as well as in deforested stream margins and selectively logged forests, and to provide bridge habitat between the large forest areas of the provincial parks. These ecological restoration practices contribute to biodiversity conservation through the regeneration of the original habitats supporting biodiversity [9–10]. As modification and restoration of vegetation structure can cause changes in some populations of animal species, particularly in birds, assessing the contribution of different habitats to regional diversity is important [1112–13].

Fig. 1:

Geographic location of the studied Ecological Corridor Urugua-í – Foerster (box), between the Provincial Parks of Urugua-í (84,000 ha) and Foerster (5,000 ha) in Misiones province, Argentina.

Misiones (particularly the Atlantic Forest of Argentina) is one of the areas of highest bird diversity in Argentina [14], providing suitable habitat for several endemic species [15–16] that are of major conservation concern, at both global and national levels [17–18]. Nevertheless, research involving birds has been primarily descriptive (point records of species distribution, checklists, and scattered natural history data), and only a few studies evaluate bird diversity patterns and their underlying causes in this region and in tropical forest [2, 6, 19–20]. Among them, some studies analyzed the effects on bird communities of forest fragmentation and habitat loss caused by human activity [21222324–25] and general patterns of land use [1112–13, 2627282930–31]. These studies showed that the loss of structural components of old-growth forest (such as old living trees and logs) reduces bird richness and changes the composition of bird communities [11, 13, 31], which is related to species' dependency on forested habitats [25, 31]. Therefore, the most transformed habitat would have low bird richness and a composition of generalist bird species or non-forest-dependent bird species. Forest-dependent, endemic and threatened bird species are strongly affected by fragmentation [26, 31]. Their vulnerability to fragmentation creates a need to conserve large remnants of native forest to preserve the high biodiversity of Atlantic Forest birds [26]. Ecological corridors are a useful conservation strategy to provide functional connectivity between forest remnants and increase their biodiversity, but there have not been many studies of biodiversity in ecological corridors in the tropics and subtropics [32–33].

As at a regional scale, the ecological corridor has a variable number of habitat types that combine into a heterogeneous landscape. The study of alpha, beta and gamma components of the diversity are useful for measuring and monitoring the effects of human activities on biodiversity, such as fragmentation [3435–36]. Studying the relationships and the factors that determine the structure and composition of bird communities provides helpful information about the alteration of the environment and species populations by human activities [37]. The study of bird community attributes can reveal the variation of local diversity (alpha diversity) and the complement of species composition among sites within the region (beta diversity), and how these diversities contribute to regional diversity (gamma diversity) [35, 37]. The influence of alpha and beta diversities on gamma diversity is an essential aspect of local and landscape level conservation plans [38]. The relationship of alpha and beta diversities with gamma diversity in a modified landscape depends on its homogeneity [35, 38]. In fragmented or heterogeneous tropical landscapes the number of species (related to gamma diversity) is superior to that observed in the richest of these habitats (alpha diversity), due to a strong complement between different habitat types (beta diversity) [35, 38].

In this study, we provide a thorough description of the bird community in the ECU-F, based on its main attributes (specific composition, richness, abundance, and evenness), taking into account the concept of alpha, beta and gamma diversity [34–35]. Our objectives were to compare how well the main habitat types in the ecological corridor provide habitat suitable for bird diversity, and the influence of alpha and beta diversities on gamma diversity. We evaluate the composition of each habitat by determining the number of generalist and specialist species. The study includes contrasting climate conditions (winter and summer), to determine whether there is a seasonal variation in alpha, beta and gamma diversities, mainly from the presence of bird migrant species. Finally, we provide management recommendations for preserving biodiversity in the studied corridor and in the surrounding area.

Methods

Results

We recorded a total of 1,207 individual birds (representing 123 species). A total of 104 species were found in MF, 45 in SF and 20 in G (Appendix 1). The rarefaction curves showed that the expected bird richness, at the same sampling size, present a pattern where MF has the highest bird richness, with expected species numbers of 42.6 and 48.8 during summer and winter respectively, followed by SF, with expected species numbers of 27 and 32. G has the lowest bird richness with expected species numbers of 15.7 and 12.6 (Fig. 2). The mean alpha diversity and its components (mean richness, mean evenness and mean abundance) showed a similar pattern as well in both seasons, with MF reaching the highest values, followed by SF and G (Figs. 3–4).

Fig. 2:

Rarefaction curves based on the expected number of bird species for the three studied vegetation types ± SD during winter (a) and summer (b), in the Ecological Corridor Urugua-í – Foerster, Argentina.

Fig. 3:

Values of mean alpha diversities N1 (a) and N2 (b), and mean bird richness (c) ± SE estimated in each studied vegetation type in each contrasting season: winter and summer, in the Ecological Corridor Urugua-í – Foerster, Argentina. Means with same letter are not significantly different (p > 0.05).

Fig. 4:

Values of community attributes at alpha level of mean evenness (a) and mean species abundance (b) ± SE, estimated for each studied vegetation type regardless of the season, in the Ecological Corridor Urugua-í – Foerster, Argentina. Means with same letter are not significantly different (p >0.05).

The “optimal” model selected with GLM (Appendix 2) found significant differences, mainly between MF and G in N1 and N2 diversities (AIC = 608.83, F_2,56 = 3.95, p = 0.0248 and AIC = 692.72, F_2,38 = 3.26, p = 0.0300, respectively) and mean richness (AIC = 639.75, F_2,56 = 3.57, p = 0.0348), in both studied seasons (Fig. 3). The mean evenness was relatively high in each vegetation type, and significant differences were found between MF and G (AIC = 245.66, F_2,54 = 4.87, p = 0.0118), regardless of the season (Fig. 4a). Fifty-seven species were forest specialist species (55 of them were found in MF and 15 in SF), 48 generalist (44 were found in MF, 25 in SF, and six in G), 11 edge species (five were found in MF, five in SF and seven in G) and seven grassland specialist species (all of them in G) (Appendix 1). The mean abundance presented significant differences between MF and the other two studied vegetation types (AIC = 767.03, F_2,57 = 3.81, p = 0.0281) (Fig. 4b).

A possible seasonal variation in bird diversity was obtained (AIC = 608.83, F_2,56 = 3.95, p = 0.0248 and AIC = 692.72, F_2,38 = 3.26, p = 0.0300 to N1 and N2 respectively), but this variation was observed only in the most diverse vegetation type, MF, which had high values during winter (Fig. 3a–3b). The same result was obtained for the mean bird richness (AIC = 639.75, F2,56 = 3.57, p = 0.0348), in which SF showed a possible temporal variation as well (AIC = 639.75, F_2,56 = 3.57, p = 0.0348) (Fig. 3c). Nevertheless, the bird mean evenness and mean abundance did not show a seasonal variation (AIC = 245.66, F_2,37 = 2.08, p = 0.1392 and AIC = 767.03, F_2,56 = 0.98, p = 0.3818, respectively).

At beta level, G and MF were the vegetation types with highest difference, or lowest degree of similarity in bird species and relative abundance, in all coefficients of similarity estimated in both seasons (Table 1). G shared 4.2% of species (five out of 119 species) with MF, and 10.2% of species (six out of 59 species) with SF, regardless of season. Otherwise, the most similar vegetation types were MF and SF, though not markedly, sharing 35.4% of species (39 out of 110 species), regardless of season (Table 1).

Table 1.

Coefficients of similarity estimated, as beta diversity, among the three studied vegetation types: mature forest (MF), secondary forest (SF) and grassland (G), for the two contrasting seasons, in the Ecological Corridor Urugua-í – Foerster, Argentina.

At landscape level (gamma), we found higher values in alpha diversity than beta diversity in both seasons (Table 2). The Shannon index suggested that gamma diversity is particularly affected by alpha diversity (about 85%), and to a lesser extent, by beta diversity (15%) in both winter and summer. Simpson index values showed a similar trend, with alpha and beta diversity contributing 98% and about 2% to gamma diversity, respectively (Table 2). Seasonal variation in alpha, beta and gamma diversities apparently was not observed (Table 2).

Table 2.

Values of alpha, beta and gamma diversities based on Shannon index (Hʹ) and Simpson index (lgr;ʹ), for the two studied contrasting seasons, in the Ecological Corridor Urugua-í – Foerster (Misiones, Argentina). Also, the contribution of alpha and beta diversities to gamma diversity is shown in percentage for each index estimated.

Discussion

The bird diversity pattern that we found in the Ecological Corridor Urugua-í – Foerster (ECU-F) is congruent with the gradient of vegetation conditions, determined by the three characteristic vegetation types described. These vegetation types, or habitat types for birds, represent different levels of anthropogenic disturbance or successional stages of the mature forest under restoration: mature forest (MF), secondary forest (SF) and grassland (G). This pattern is caused by variation in bird specific richness and evenness. The structure and heterogeneity of vegetation, as well as its vertical stratification in the different vegetation types, seem to be the most important factors influencing the diversity pattern of birds, as some authors propose [6364–65]. In the ECU-F, this is reflected mainly in the differences between G and MF, with the latter showing the highest internal heterogeneity not only by its greater variety in types and composition of components, but also by its functional and structural relationships both vertically and horizontally, providing greater structural complexity [4, 6] and higher bird diversity.

However, the differences in diversity mainly between MF and SF probably are best explained by the loss of structural components that reduce complexity. The loss of bird richness is mainly due to the loss of specialist or forest-dependent species, which are the most sensitive to the replacement of natural forest [54]. The most forest specialist species were found in the MF (53% of its avifauna), whereas the bird assemblage of SF was composed mainly of generalist species (55% of its avifauna) and forest specialist species (33%) (Appendix 1). Similarly, other studies in the Atlantic Forest of Argentina [26, 31] showed that the observed decline in bird richness was related to species dependence in forested habitats to differences among forest habitat types [31], and to different area sizes of native forest fragments [26]. We recorded 33 endemic species, of which 27 are forest specialist and three are endemic and globally threatened: Helmeted woodpecker (Dryocopus galeatus), Blackish-Blue Seedeater (Amaurospiza moesta) and Southern Bristle-Tyrant (Phylloscartes eximius) [66].

The evenness contributes to the diversity pattern obtained, as stated above. We found high values of this community attribute in MF and in second place in SF, where two or more species co-dominate in the community (e. g. White-rimmed Warbler (Basileuterus leucoblepharus) and Plush-crested Jay (Cyanococorax chrysops)). In contrast, G had a lower value, and few bird species dominate in this habitat (e. g. Smooth-billed Ani (Crotophaga ani)) (Appendix 1).

The possible seasonal variation in alpha diversity (N1 and N2), mainly in the MF, reflects a potential dependence on the diversity with the season. In other words, the values of bird diversity vary between winter and summer, showing high values during winter in the mature forest. This variation is probably due to changes in richness, which showed a temporal variation as well. However, this change in richness is not due to the presence of migrant species. When the species composition is analyzed, it shows that migrant species, such as Greater Ani (Crotophaga major), Black-crowned Tityra (Tityra inquisitor), Fork-tailed Flycatcher (Tyrannus savanna) and Boat-billed Flycatcher (Megarhynchus pitangua) are relative few compared to resident species. These birds nest in spring-summer and migrate north during autumn. In contrast, we found high values of richness during the most unfavorable season, perhaps because in winter many species search for the favorable shelter conditions provided by a more forested or dense vegetation type. Moreover, in winter they congregate in mixed-species flocks for foraging, concentrating more species in one sample.

At beta level, first of all, we found that results coincide with those found at alpha level or local scale. Thus, the highest difference in species composition was between MF and G, suggesting that each habitat has its own bird species composition, while SF and MF were the most similar, regardless of the season. Second, because beta diversity is related to environmental heterogeneity, we expected higher values in tropical fragmented landscapes because of the dissimilarity of habitats [35, 38]. On the contrary, we found lower values (compared with alpha diversity), which are probably because there are more forest-dependent than forest-generalist bird species [37]. In addition, the mature forest is a large fragment of continuous forest that is in contact with the Horacio Foerster and Urugua-í Provincial Parks, providing a more homogeneous area for birds in the studied ecological corridor.

The gamma diversity of birds seemed to be more affected by alpha diversities than by the beta component, contrary to other studies [35, 37] in which regional or landscape diversity of tropical or fragmented forests was mainly determined by beta diversity both in birds [37] and in some mammals [35]. However, as some authors propose [35, 37, 38], this relationship seems to depend not only on the scale, but in the response to habitat variability and to the dispersal capacity of the studied taxonomic group. For example, a study of bats conducted in a fragmented landscape of Latin American rainforest found that regional diversity depends on local diversity [38], as in our study. Thus, the MF, with higher richness, was likely to make the greatest contribution to regional diversity, followed by SF and finally by G. In SF we found the some but not all of the same species as in MF. The G showed species totally different from the most preserved habitat, which would increase the regional bird diversity as well. This result is expected in homogeneous landscapes or where anthropogenic changes have impoverished the original habitat type [38]. Therefore, the studied ecological corridor, an area with different vegetation types or habitats, is in fact a homogeneous area for birds.

Although it was not statistically tested, this trend appeared to be similar in both winter and summer. Consequently, the MF (like other types of recovered forests) provides habitat suitability, potentially including connectivity, to the largest number of birds. Although this study was conducted at a local level and represents a small area of the Atlantic Forest, our results have implications for future conservation plans in other areas of the Atlantic Forest ecoregion.

Implication for conservation

The ECU-F showed a high richness of birds, including an important number of endemic species of the Atlantic Forest, some of which are forest specialists and globally threatened (e. g. Helmeted woodpecker (Dryocopus galeatus), Blackish-Blue Seedeater (Amaurospiza moesta) and Southern Bristle-Tyrant (Phylloscartes eximius)) (Fig. 5). Our results confirm the great need for conservation of both secondary and native forest in this area and other tropical forest fragments of Atlantic Forest subjected to anthropogenic activities such as selective logging and agriculture.

Fig. 5:

Iconic bird species documented in the Ecological Corridor Urugua-í – Foerster, Argentina, which are endemic in the Atlantic Forest and most of them are threatened. A. Helmeted woodpecker (Dryocopus galeatus) (by Jorge La Glotteria), B. Bay-ringed Tyrannulet (Phylloscartes sylviolus) (by the third author Julián Baigorria), C. Blackish-Blue Seedeater (Amaurospiza moesta) and D. Shouthern Bristle-Tyrant (Phylloscartes eximius) (both by Roberto Güller).

Our results point to alpha diversity as the main component to be preserved for maintaining species diversity in the ECU-F, with particular focus on the MF due to its high values in this parameter and in bird richness. Furthermore, MF (and other degrees of recovered forests) should be especially considered in management plans for the Atlantic Forest, first because it has several forest specialist bird species, most of them endemic and some threatened. Second, it is the most threatened environment due to past and current anthropogenic activities.

Ecological corridors increase the functional connectivity between protected remnants of habitats, a benefit to forest dependent species (also species of other taxa), increasing the mobility of individuals between habitat patches in constantly changing landscapes. Ecological restoration should therefore continue in the studied corridor and in other areas of the Atlantic Forest, creating new corridors between reserves, which will effectively enhance conservation of biodiversity at the macro-regional scale. We also recommend proper management of native forests, with the identification of suitable indicator bird species for natural habitats, to monitor the success of ecological restoration measures in the region. Proper design of ecological corridors, with suitable habitat conditions and free circulation of wildlife and native vegetation [67686970–71], may ensure the preservation of biodiversity in the Atlantic Forest and its environmental services in the medium and long term.