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Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil

Twenty-three years of bird monitoring reveal low extinction and colonization of species in a... Revista Brasileira de Ornitologia, 24(3), 235-259 ARTICLE September 2016 Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil 1,5 1 2 3 Guilherme Willrich , Larissa Corsini Calsavara , Marcos Robalinho Lima , Renan Campos de Oliveira , 1 1 4 2 Gabriela Menezes Bochio , Gabriel Lima Medina Rosa , Vanildo Cesar Muzi and Luiz dos Anjos Programa de Pós Graduação em Ciências Biológicas, Universidade Estadual de Londrina, CEP 86051-990, Londrina, PR, Brazil. Laboratório de Ornitologia e Bioacústica, Departamento de Biologia Animal e Vegetal, Universidade Estadual de Londrina, CEP 86051-990, Londrina, PR, Brazil. ONG MAE - Meio Ambiente Equilibrado, Rua Goiás, 1774, CEP 86010-465, Centro, Londrina, PR, Brazil. Rua Japuguaçu, 234, CEP 86702-236, Jardim Bela Vista, Arapongas, PR, Brazil. Corresponding author: guigawillrich@hotmail.com Received on 04 November 2015. Accepted on 11 September 2016. ABSTRACT: Human activities have modified landscapes worldwide, promoting fragmentation and isolation of forest habitats. Such landscape modifications are responsible for changes in species composition due to extinction and colonization events. Forest species dynamism is usually affected by forest fragmentation when remaining fragments are small and isolated, but forest dynamism is usually more stable when forest fragments are large and connected. In this study we verified c hanges in bird composition during 23 years of bird monitoring at the Mata dos Godoy State Park (PEMG). We aimed to evaluate the avian community dynamism of this reserve, as well as its effectiveness in protecting biodiversity in an extremely fragmented landscape. We reviewed historical records of bird species composition and checked for any possible misidentifications, updated t he list and created an annual data set of bird species occurrence. We used this list to evaluate species persistence, species loss, and colonization over the study period. Additionally, species were classified accor ding to their guilds in order to determine which species traits were associated with local extinction. A total of 331 bird species were recorded in PEMG over 23 years of monitoring, 17 of which were considered locally extinct or possibly extinct, and 11 were recent local colonizations. This indicates that bird composition in PEMG has been relatively stable over the years. However, local extinction was more likely for large frugivores and insectivores, which are guilds already known to be more susceptible to local extinction. Colonizations, in turn, were associated with guilds of more open habitats, like edge insectivores. We suggest that extinctions and colonizations are also potentially related to species distribution ranges and climate change. Although local extinctions occurred, PEMG still maintains a significant fraction of its historical avifauna and may potentially maintain source populations for many bird species, thus making it an important reserve for the north of Paraná. KEY-WORDS: avifauna, Atlantic Forest, forest fragment dynamism, Protected Area, species persistence. INTRODUCTION ha (Ribeiro et al. 2009) and surrounded by a matrix of anthropogenic habitats (e.g. plantations and urban areas) Human activities, such as food and energy production, are (Tabarelli et al. 2010). responsible for the modification of landscapes worldwide The Atlantic Forest Biome consists of several different forest formations that have suffered different deforestation (Foley et al. 2005, Sodhi & Ehrlich 2010, Haddad et al. 2015). These activities contribute to changes in climate pressures (Galindo-Leal & Câmara 2003). In the north regimes, loss of ecosystem services such as air and water of Paraná state (southern Brazil), which is comprised by quality and decrease in forest cover, all of which result in semi-deciduous forest formations, deforestation has led biodiversity loss (DeFries et al. 2004, Foley et al. 2005, to the loss of approximately 98% of the original forest cover (Torezan et al. 2005). In this landscape scenario, Zhao et al. 2006, Haddad et al. 2015). In the Atlantic Forest Biome, a biodiversity hotspot (Myers et al. 2000), however, Mata dos Godoy State Park (Parque Estadual this scenario is alarming because only 11.4% to 16% of Mata dos Godoy - PEMG) stands out as potentially the the original forest cover still remains (Ribeiro et al. 2009). most important reserve since it is the largest and most Exacerbating this situation is the fact that the majority well preserved forest fragment in the north of Paraná state (Anjos et al. 2007, 2009). Even though this reserve is of the remaining forest fragments are smaller than 50 Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. immersed in an agro-mosaic matrix, much of the regional are an important component to determine the persistence, fauna of anurans (Bernarde & Anjos 1999, Machado & colonization and/or local extinction of species. However, Bernarde 2006), reptiles (Bernarde & Machado 2006) and before using this type of data it is important to review birds (Anjos et al. 1997, Anjos 2001) are well represented the historical records of the literature to guarantee in PEMG. Also, PEMG contains 21 threatened species that the data does not contain dubious records (i.e. and 15 rare species of Angiosperms (Rossetto & Vieira misidentification). Lees et al. (2014) suggest several ways 2013), which makes PEMG an important reserve for of dealing with misidentification. For instance, one could semi-deciduous forest formations. In fact, this protected use the distributional range of the species in question area has become a regional conservation reference not only to determine if it overlaps with the dubious record, or because of its intrinsic biological value, but also because one could possibly determine if suitable habitat for of the development of several environmental educational the species occurs in the area in question, or even the programmes with local communities. possibility of a mix up between very similar species (e.g. Despite its importance for regional conservation, Drymophila ferruginea and D. rubricollis). We have two PEMG still suffers several t hreats. The biggest threat to goals for this study, the first one to present a revised PEMG is the expansion of agriculture, which has taken historical checklist for the birds of PEMG, where we place in the last seven decades, but others threats such present species occurrence data from 1993 to 2015 and as illegal hunting, invasive species and water pollution check for possible misidentifications. Our second goal is are also present (IAP 2002). At the landscape level, the to use this revised checklist to assess the potential species continuation of habitat loss has led to an increase in forest dynamism in this reserve during the last 23 years. Because fragmentation and its associated negative outcomes, such as birds are recognized as good biological indicators and edge effects and forest fragment isolation. These landscape capable of responding to primary and secondary causes modifications could have important consequences for of environmental changes (Morrison 1986, Temple & forest fragment dynamism (Laurance 2002). According to Wiens 1989, Koskimies 1989, Kushlan 1993, Piratelli et the concept of forest fragment hyperdynamism, small and al. 2008), our approach will allow us to determine how isolated areas tend to be strongly affected by the impacts of effective P EMG is for the conservation of the regional fragmentation in a short time frame and should present, biota in the north of Paraná state. for example, high species turnover (Laurance et al. 1998, Laurance et al. 2002). Conversely, large connected forest METHODS fragments tend to suffer fewer changes in the same short time frame with a weak dynamism, because it will usually harbor a higher number of persisting species (Bierregaard Study area et al. 1992, 1998, 2002, Laurance 2010). Laurance (2002) suggested that forest fragmentation tends to Mata dos Godoy State Park (23°27'S; 51°15'W, PEMG, Figure 1) is the largest and best preserved forest fragment affect the dispersion of species and individuals, leading to an increase in colonization of generalist, invasive and in northern Paraná state, south of Brazil (Anjos et al. pathogenic species, which will usually modify biological 2007). PEMG is located in Espírito Santo District, 15 km interactions (i.e. through competition). These in turn from the center of the municipality of Londrina and over will affect both species abundance and composition the Tropic of Capricorn. This reserve covers 656 ha and is mainly composed by pristine seasonal semi-deciduous (Bierregaard et al. 1992, Laurance et al. 2002, Laurance 2002, 2010). However, the effects on forest dynamism forest (Figure 1, Torezan 2002). PEMG presents a natural will depend on the duration and strength of these and variation in topography, which allows one to divide other impacts, and on the characteristics of the forest PEMG in two different regions comprised of pristine fragment (Laurance 2002, Laurance et al. 2002). At forest. One of the regions is located in the north and consists of a plateau at an altitude of approximately 600 m, the moment, it is uncertain if PEMG has maintained its biodiversity over the years. Therefore, it is crucial to while the second region is located in the south of PEMG document how species composition has changed since and consists of a hillside that ranges from 600 to 470 m PEMG became a legal reserve to assess its current and a.s.l. (Anjos et al. 2007). This difference in elevation is future role in the protection of biodiversity. Moreover, responsible for the widespread occurrence of bamboo vegetation in the southern part of PEMG, which results this will provide a better understanding of which species are more susceptible to local extinction in semi-deciduous in differences in the occurrence of bir d species between forest formations of the Atlantic Forest. these two areas (see Anjos et al. 2007, Santana & Anjos In this study we verified if the bird community of 2010). For more details on the vegetation of PEMG see PEMG has been maintained over the years after it was Silveira (2006) and Rossetto & Vieira (2013). This reserve also harbor an area of secondary forest in the southeast, an recognised as a legal reserve in 1989. Historical data sets Revista Brasileira de Ornitologia, 24(3), 2016 Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. area of open habitats (e.g. pasture or initial regeneration) review because bird data from these specific studies had in the northern portion, and a reforestation area that was already been published in one of the ten references listed implemented twenty years ago (IAP 2002; Figure 1). in Table 1. TABLE 1. Published bird occurrence data in PEMG, Paraná state, Brazil, and the respective period in which fieldwork was conducted. Published papersPeriod of field wor k Anjos et al. 1997 1992–1996 Anjos & Ferreira 1998 September 1997 Anjos 2001 January–December 1996 Anjos et al. 2004 September–December 1997 Anjos et al. 2007 September–December 2001 Lopes et al. 2006 2003–2004 Anjos et al. 2011 2004–2005 Santana & Anjos 2010 2007 Bochio & Anjos 2012 2009–2010 Zaiden et al. 2015 2010–2011 Unpublished data, in turn, consisted of different methodologies and sampling efforts that were conducted between 1993 and 2015, these methods were: ad libitum searches, point counts, and bird capture with mist nets. Ad libitum searches by different observers were conducted in the entire area of PEMG without controlling for sampling effort. Point counts (Vielliar d & Silva 1990, Bibby et al. 1993) were performed in PEMG during three different periods: (1) 1993–2002, (2) 2004–2005, and (3) 2014. For the first period, point counts were FIGURE 1. Location of Mata dos Godoy State Park (PEMG, 23°27'S; conducted in 1993, 1995–1999, 2001 and 2002. In 51°15'W) in the north of Paraná state, south of Brazil. each of these years, with the exception of 1996, five A matrix of privately owned agricultural land point counts in pristine forest were sampled twice during surrounds the northern and western borders of PEMG, spring (October). In 1996, the same point counts were while the Apertados River borders the south and a performed once a month from January to December continuous forest fragment borders the east. Considering (Anjos 2001). Point counts in all these years (including all forest fragments surrounding PEMG up to a distance 1996) were placed 100 m apart and at least 50 m away of 1 km, connected or not to PEMG, there is a mosaic from the forest edge (Figure 1). Sampling time for each of forest cover of approximately 2800 ha (Lopes et point was 20 minutes, and the radius of detection was al. 2006). PEMG is situated in the Tibagi River basin unlimited. For the second time period, point counts (IAP 2002) and according to Köppen classification, the were conducted every season in 2004 and 2005. In this climate of the region is Cfa, subtropical humid with case, six point counts along two trails were placed 200 rainy summers, average yearly temperatures of 21°C and m apart, giving a total of 12 points (Figure 1). Point average maximum and minimum temperatures of 28°C counts were sampled for 15 minutes with a detection and 16°C, respectively. radius ≤100 m (Anjos et al. 2011). Data from spring and summer from this second time period were published Data set in Anjos et al. (2011, 2015), but for the present study we have also incorporated unpublished records from The historical data set was obtained using both the autumn and winter. The thir d point count sampling scientific literature and unpublished data. From the period occurred from September to December 2014. In scientific literature, we compiled data on bird species this case, 39 point counts (with 15 min sampling time using ten scientific papers published between 1997 and and a detection radius ≤50 m) were placed along 13 2015 (Table 1). Several studies (e.g. Anjos & Schuchmann trails, each trail consisted of three point counts at 200 1997, Anjos et al. 2010) were excluded from the literature m intervals (Figure 1). Each point count was sampled Revista Brasileira de Ornitologia, 24(3), 2016 Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. four times during the sampling period. In all of the during the entire study period and for which PEMG three-time periods, bird sampling was conducted early harbor suitable habitat for the specie. For the last case in the morning and started with species vocal activity. we were unable to classify the species as persistent, Sampling ended approximately 3 h later. extinct or colonizer. Classification into forest, non-forest Mist nets were placed in six different locations in and migrant species follows Sick (1997), del Hoyo et PEMG between February and October 2015 (Figure 1), al. (2015) and our personal observations in the study with a total sampling effort of 10,332 h.m . Mist nets area. For species that were mentioned in the literature as procedures followed Roos (2010). both forest and non-forest, we used the habitat that was Bird nomenclature and systematic classification are described as preferred for the species. in accordance with the list of Brazilian birds reviewed and The Sørensen Index of Similarity (Magurran 1988) updated by the Comitê Brasileiro de Registros Ornitológicos was used to analyse variation in species composition (Piacentini et al. 2015). The conservation status of each over time. We used this index to calculate how similar species was based on IUCN (2015), ICMBio (2014) the two time periods were (before 2005 and after 2005). and Mikich & Bérnils (2004) at the global, national and The following formula was used to calculate the Sørensen regional levels, respectively. We used Bencke et al. (2006) Index of Similarity: Ss = 2j / (a + b); where j corresponds to classify species as endemic to the Atlantic Forest. to the number of species common to both periods (before 2005 and after 2005), a represents the number of species Data analysis present before 2005 and b the number of species present after 2005 (Magurran 1988). For this analysis we first The data set was organized on an annual basis and pooled the species in the categories “extinct”, “possibly bird records were divided into two larger time periods, extinct”, “forest persistent”, “non-forest persistent”, before and after 2005 (Appendix I). We only considered “forest persistent and declining” and “colonizer”. We then presence and absence data because sampling effort among excluded “colonizer” species in order to verify only the studies, from the scientific literature or unpublished data, effects of extinctions over the periods. were not standardized, making quantitative comparisons In order to evaluate if certain traits made the unfeasible. Based on this list, we carefully reviewed species more prone to extinction, species were grouped questionable records (e.g. misidentifications) in or der to according to their guilds. Species were classified using a eliminate “false presences”. This procedure allowe d for the combination of food resources explored by the species correct evaluation of local species persistence in PEMG and habitat choices, which were mainly based on Willis (Lees et al. 2014) according to the categories presented (1979), Ribon et al. (2003), Giraudo et al. (2008) and below. our own field o bservations. Species were classified as: We categorized bird species as: 1) “forest persistent”, carnivores (CA); carrion eaters (CE); large frugivores forest bird species that were recorded regularly in the (LF); small frugivores (SF); seedeaters (SE); nectarivores entire study period; 2) “non-forest persistent”, species (NE); ground insectivores (GI); understory insectivores that inhabit non-forest habitats and were recorded (UI); trunk and twig insectivores (TI); sub-canopy and regularly in the entire study period; 3) “forest persistent canopy insectivores (SCI); aerial insectivores (AI); edge and declining”, forest species that were recorded regularly insectivores (EI); nocturnal insectivores (NI); ground up to 2005, but were only recorded in one or two years omnivores (GO); understory omnivores (UO); sub- after 2005; 4) “possibly extinct”, forest species that were canopy and canopy omnivores (SCO); edge omnivores regularly recorded until 2005, but were not recorded (EO); aquatic omnivores (AO); and piscivorous (PI). thereafter; 5) “extinct”, forest species that were regularly To visualize which guilds increased or decreased in recorded until 2000, but not afterwards, or species number of species during the last 23 years in PEMG, that are easily detectable (e.g. Odontophorus capueira) we plotted a graph with the number of species in each but were recorded only in the first years of monitoring guild that were present before and after 2005. For this (1993–1996); 6) “frequent migrants”, migrant species in analysis, we excluded the following categories: “frequent the south of Brazil that were present during most of the migrant”, “occasional migrant”, “sporadic species” and studied years; 7) “occasional migrants”, migrant species “indeterminate”. We considered a species to be declining that were occasionally found during the study period; and in risk of future extinction when it presented a decline 8) “colonizer”, species that were found in consecutive in occurrence records after 2005. We used this data to years in the study area after 2005 and not before; 9) determine the future tendency in the number of species “sporadic species”, species for which PEMG harbor for each guild. Future tendency of a guild was defined as unsuitable habitat (e.g. Ardeidae) and that had few and the number of species present after 2005, subtracting the infrequent records during the entire study period; 10) number of species in the category “forest persistent and “indeterminate”, species with few and infrequent records declining” (Figure 2). Revista Brasileira de Ornitologia, 24(3), 2016 Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. considered locally extinct, five species as possibly extinct Before 2005 After 2005 and 11 species were considered to be recent colonizations, Future tendency according to our criteria (Table 2). For the remaining species, 42 species were considered migrants (30 frequent and 12 occasional) and 70 were recorded only once or twice during the monitoring period (37 classified as sporadic and 33 as indeterminate; Appendix I). A total of 28 bird species (~10%) were considered either as locally extinct, possibly extinct or persistent and declining. Moreover, of the 13 species considered threatened at global, national or regional levels recorded in PEMG during the entire monitoring period, seven are CA CE LF SF SE NE GI UI TI SCI AI EI NI GO UO SCO EO already locally extinct or possibly extinct and three others Guild are considered to be declining (Table 2). Three species FIGURE 2. Number of species before and after 2005 for each bird considered near threatened at regional and global levels guild in Mata dos Godoy State Park (PEMG), Paraná state, Brazil. Only the following categories were considered: “extinct”, “possibly were also considered locally extinct in PEMG. However, extinct”, “colonizer”, “persistent and declining” and “persistent”. two species, Myiothlypis flaveo la and Nyctiphrynus For the latter category, both forest and non-forest bird species were ocellatus, which are threatened bird species at the regional considered. Species that presented a decline in occurrence records after level, were considered to have recently colonized PEMG. 2005 were considered to be declining and in risk of future extinction and this data were used to determine the future tendency in the If we exclude the species that went locally extinct, PEMG number of species for each guild. Guild: CA – carnivores; LF – large currently harbor 319 bird species (68 endemic to Atlantic frugivores; SF – small frugivores; SE – seedeaters; NE – nectarivores; Forest), out of which eight are threatened species, 16 near GI – ground insectivores; TI – trunk and twig insectivores; SCI – threatened and five data deficient for the Paraná state sub-canopy and canopy insectivores; EI – edge insectivores; NI – (Appendix I). nocturnal insectivores; GO – ground omnivores; SCO – sub-canopy and canopy omnivores; EO – edge omnivores. The most representative guilds, considering the total number of bird species originally recorded at RESULTS PEMG (331), were edge omnivores (n = 36, 10.9%), understory insectivores (n = 31, 9.4%), sub-canopy and A total of 331 bird species were recorded during 23 years canopy insectivores (n = 30, 9.0%), edge insectivores of bird monitoring in PEMG (Appendix I). Thirteen (n = 28, 8.4%), large frugivores (n = 26, 7.8%), sub- species found in the literature review were not included canopy and canopy omnivores (n = 23, 6.9%), trunk in this list of 331 bird species, either because their ranges and twig insectivores (n = 22, 6.6%) and carnivores (n did not include northern Paraná, or because they were = 22, 6.6%) (Appendix I). In general, insectivores were recorded only once and could represent dubious records highly representative with 149 species (45.0%), followed (Appendix II). Of the 331 species with confirmed by omnivores (84, 25.4%) and frugivores (35, 10.6%). presence in PEMG, 74 species are endemic to the Atlantic The two guilds with t he highest number of species Forest, while 13 species are considered threatened either going locally extinct were large frugivores (33.3%, n = 4) at the global, national or regional levels (Appendix and ground omnivores (16.6%, n = 2) (Table 3). Possibly I). Furthermore, 19 species are considered “Near extinct species were mainly represented by sub-canopy and threatened” at global and regional levels, and five species canopy insectivores (40%, n = 2). Large frugivores had the are considered as “Data deficient” in the Paraná state. highest number of forest bird species that are declining Bird community composition before and after 2005 (27.2%, n = 3), followed by ground insectivores (18.2%, n was very similar (93%; Ss = 0.932). When colonizer = 2). Colonizers, on the other hand, were well represented species were excluded, bird species similarity between the by the insectivores and omnivores guilds (Table 3). two time periods increased (95%, Ss = 0.957), as expected. Large frugivores are expected to have a higher number Therefore, P EMG presented a stable avifauna during the of future local extinctions because of the decline in the 23 years of bird monitoring. However, the number of number of species occurrence for this category (Figure 2). species that went extinct promoted a higher dissimilarity Small frugivores, ground insectivores, ground omnivores, (5%) between the two time periods than the number of trunk and twig insectivores, as well as sub-canopy and species that later colonized PEMG (2%). This stability canopy insectivores were guilds that had a high number was expected because 191 out of the 331 species, that were of species at risk of local extinction. Conversely, edge originally found in PEMG, were considered as persistent insectivores, edge omnivores, nocturnal insectivores and (150 forest persistent, 30 non-forest persistent and 11 nectarivores tended to maintain local populations and may forest persistent and declining), while only 12 species were even see increases in the number of species in the future. Revista Brasileira de Ornitologia, 24(3), 2016 Number of species Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. TABLE 2. Species considered extinct, possibly extinct, declining and recent colonisers in PEMG, Paraná state, Brazil. Local Status: EX – extinct; PE – possibly extinct; D – forest persistent and declining; C – colonizer. Conservation Status: VU – vulnerable; EN – endangered; CR – critically endangered; NT – near threatened; DD – data deficient; PR – regional level (Mikich & Bérnils 2004); BR – national level (ICMBio 2014); GL – global level (IUCN 2015). Guild: CA – carnivores; LF – large frugivores; SF – small frugivores; SE – seedeaters; NE – nectarivores; GI – ground insectivores; TI – trunk and twig insectivores; SCI – sub-canopy and canopy insectivores; EI – edge insectivores; NI – nocturnal insectivores; GO – ground omnivores; SCO – sub-canopy and canopy omnivores; EO – edge omnivores. Endemic species (E) follows Bencke et al. (2006). Species Local status Conservation status Guild Crypturellus undulatus (Temminck, 1815) EX CR-PR GO Aburria jacutinga (Spix, 1825) EEX EN-GL; EN-BR; EN-PR LF Crax fasciolata Spix, 1825 EX VU-GL; CR-PR LF Odontophorus capueira (Spix, 1825) EEX   GO Pulsatrix perspicillata (Latham, 1790) EX VU-BR; DD-PR CA Chamaeza ruficauda (Cabanis & Heine, 1859) EE X   GI Manacus manacus (Linnaeus, 1766) EX   SF Lipaugus lanioides (Lesson, 1844) EEX NT-GL; NT-PR LF Procnias nudicollis (Vieillot, 1817) EEX VU-GL LF Phylloscartes eximius (Temminck, 1822) EEX NT-GL SCI Tiaris fuliginosus (Wied, 1830) EX   SE Piranga flav a (Vieillot, 1822) EX NT-PR SCO Tinamus solitarius (Vieillot, 1819) E PE NT-GL; VU-PR GO Campephilus melanoleucos (Gmelin, 1788) PE   TI Piprites chloris (Temminck, 1822) PE   SCI Hylophilus poicilotis Temminck, 1822 E PE   EI Polioptila lactea Sharpe, 1885 E PE NT-GL; EN-PR SCI Patagioenas plumbea (Vieillot, 1818) D   LF Strix hylophila Temminck, 1825 E D NT-GL CA Pteroglossus aracari (Linnaeus, 1758) D VU-PR SCO Piculus aurulentus (Temminck, 1821) E D NT-GL TI Primolius maracana (Vieillot, 1816) D NT-GL; EN-PR LF Triclaria malachitacea (Spix, 1824) E D NT-GL; VU-PR LF Grallaria varia (Boddaert, 1783) D   GI Hylopezus nattereri (Pinto, 1937) E D   GI Heliobletus contaminatus Berlepsch, 1885 E D   SCI Oxyruncus cristatus Swainson, 1821 D   SCO Euphonia pectoralis (Latham, 1801) E D   SF Leptodon cayanensis (Latham, 1790) C   CA Buteo brachyurus Vieillot, 1816 C   CA Nyctiphrynus ocellatus (Tschudi, 1844) C EN-PR NI Hydropsalis parvula (Gould, 1837) C   NI Amazilia versicolor (Vieillot, 1818) C   NE Amazilia lactea (Lesson, 1832) C   NE Myiarchus ferox (Gmelin, 1789) C   EI Myiarchus tyrannulus (Statius Muller, 1776) C   EI Myiothlypis flaveo la Baird, 1865 C VU-PR EI Thlypopsis sor dida (d'Orbigny & Lafresnaye, 1837) C   EO Haplospiza unicolor Cabanis, 1851 E C   SE Revista Brasileira de Ornitologia, 24(3), 2016 Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. TABLE 3. Representation of guilds (%) in each category in PEMG, Paraná state, Brazil. Each column corresponds to 100% of the respective category. Guilds are as follows: CA – carnivores; CE – carrion eaters; LF – large frugivores; SF – small frugivores; SE – seedeaters; NE – nectarivores; GI – ground insectivores; UI – understory insectivores; TI – trunk and twig insectivores; SCI – sub-canopy and canopy insectivores; AI – aerial insectivores; EI – edge insectivores; NI – nocturnal insectivores; GO – ground omnivores; UO – understory omnivores; SCO – sub-canopy and canopy omnivores; EO – edge omnivores; AO – aquatic omnivores; and PI – piscivorous. Extinct Possibly extinct Forest persistent declining Forest persistent Non-forest persistent Colonizer Guild (100% = 12) (100% = 5) (100% = 11) (100% = 150) (100% = 30) (100% = 11) CA 8.3 - 9.1 4.7 13.3 18.2 CE - - - 2.0 - - LF 33.3 - 27.2 11.3 - - SF 8.3 - 9.1 2.7 - - SE 8.3 - - 1.3 13.3 9.1 NE - - - 6.7 - 18.2 GI 8.3 - 18.2 1.3 3.3 - UI - - - 18.0 - 9.1 TI - 20.0 9.1 10.7 3.3 - SCI 8.3 40.0 9.1 10.7 - - AI - - - - 6.7 - EI - 20.0 - 2.7 30.0 18.2 NI - - - 3.3 3.3 18.2 GO 16.7 20.0 - 2.0 3.3 - UO - - - 3.3 - - SCO 8.3 - 18.2 9.3 - - EO - - - 10.0 23.3 9.1 AO - - - - - - PI - - - - - - DISCUSSION reserve, especially during the turn of the century. The buffer zone that existed 23 years ago in the west portion Over the 23 years of bird monitoring, PEMG presented of the reserve is completely absent nowadays (L. Anjos, low species turnover and a high number of bird species pers. obs.). Other local threats have been detected over persisting over this time period. Local extinction of bird the 23 years of monitoring, like illegal hunting activities species, as well as colonization of novel bird species, and the presence of domestic species (e.g. cats and dogs) did occur in PEMG during this time period, but at in the study area (IAP 2002), threats that are known to low numbers. We argue that some features of PEMG have important impacts on biodiversity and community contributed to its relative stability, these being high dynamics (Wright 2005, Galetti & Sazima 2006, Campos number of bird species, large core area, and functional et al. 2007). The synergic effects of these threats could connectivity with other forest fragments (Laurance 2002, affect bird composition in the PEMG in terms of both Haddad et al. 2015), especially in the eastern area of local extinctions and colonizations (Laurance 2010). PEMG, which borders a large forest fragment (Lopes et al. 2006). The high number of species in P EMG, in Extinctions turn, could be explained by the natural heterogeneity of the pristine vegetation encountered in PEMG. Extinctions in the PEMG were biased towards specific This natural heterogeneity is probably the result of bird groups. This was expected because some biological topographic variation (plateau vs. hillside), which allows features are known to be better predictors of bird sensitivity for the coexistence of species with different ecological to fragmented landscapes (e.g. Henle et al. 2004, Anjos requirements in this reserve (Anjos et al. 2007, Santana 2006). For example, body size and feeding habits (Pizo & Anjos 2010). 2001, Ribon et al. 2003), dispersal capacity (Sekercioglu However, PEMG is surrounded by a human et al. 2002, Lees & Peres 2009) and geographical dominated landscape that has changed dramatically distribution (Kattan et al. 1994, Anjos et al. 2010). In our during the last 23 years. Agriculture (mainly soya beans) study, large frugivores had the highest rate of extinction has expanded over the years at the northern and western (33.3% of total extinctions) and higher number of species borders of PEMG, compromising the buffer zone of the expected to decline in the future. Ground omnivores and Revista Brasileira de Ornitologia, 24(3), 2016 Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. ground insectivores followed in terms of the number of PEMG, for example, lies over the Tropic of species that went locally extinct or presented a tendency Capricorn, a transitional region between Tropical and of future decline. These three guilds frequently show Subtropical regions and lies at the northern limit for several high sensitivity to habitat fragmentation (Thiollay 1992, bird species with a more southern distribution in Brazil. Ribon et al. 2003, Franz et al. 2010, Loures-Ribeiro et Likewise, it is at the southern limit for the distribution of al. 2011, Stratford & Stouffer 2015) due to certain several bird species with a more northern distribution in biological features that increase their susceptibility to Brazil. This peculiarity could explain some of the patterns local extinction. Large frugivores, for example, present of extinctions and declines. Species at the border of their low population densities and recruitment, and need distribution have higher probability of going extinct large living areas to feed on specific resource (Pizo 2001). because of the limited rescue effect (Anjos et al. 2010) Ground insectivores, in turn, appear to be sensitive and/or because species may be at their ecological and to microhabitat changes (e.g. in leaf litter depth and physiological limits (Kattan et al. 1994). PEMG is at the vegetation structure), which frequently occur in disturbed distributional range limit of nine bird species considered and fragmented habitats (Stratford & Stouffer 2013, as either locally extinct or possibly extinct, and seven 2015). Further, large frugivores and ground omnivores bird species considered to be declining. It is noticeable are frequently hunted due to their large body size (Strahl that species with a more southern distribution were & Grajal 1991, Pizo 2001), and terrestrial birds are more more affected (12 species, e.g. Heliobletus contaminatus, susceptible to predation by domestic species (e.g. dogs Lipaugus lanioides and Polioptila lactea) than species with and cats). a more northern distribution (4 species, e.g. Campephilus Other guilds that declined and had a high number melanoleucus and Crypturellus undulatus). of species that went “possibly extinct” were sub-canopy A possible factor responsible for the extinction bias and canopy insectivores and sub-canopy and canopy towards bird species with a more southern distributional omnivores, which are guilds that are usually not cited range is the drastic deforestation that occurred in Paraná as being prone to local extinction due to fragmentation state between 1890 and 1990 (Gubert-Filho 2010). (Bregman et al. 2014). Anjos (2006) studied the Deforestation in Paraná was severe for both semi- sensitivity of bird species in the fragmented landscape deciduous forests (that prevails in northern Paraná) of PEMG, and found that some particular species in the and araucaria forests (that occurs more to the south), aforementioned guilds (e.g. Piprites chloris and Oxyruncus eliminating the connectivity that once existed between cristatus) presented high local sensitivity to the effects of this two forest formations. Enclaves of Araucaria Forest fragmentation. However, understory insectivorous - a that were close to PEMG did occur in the past (Torezan guild that usually declines after forest fragmentation and 2002), but these have been eliminated or have become forest isolation (Stouffer & Bierregaar d 1995, Sekercioglu isolated from the core Araucaria Forest present in the south et al. 2002, Powell et al. 2015) - persisted in stable of Brazil. Thus, bir d species highly associated to Araucaria numbers in PEMG. A possible explanation could be Forest that occur in PEMG could be disappearing or the fact that we considered terrestrial species as “ground declining due to the lack of suitable habitats and absence insectivores” instead of grouping them as “understory of landscape connectivity that could allow a rescue effect. insectivores”. We think it is important to consider where This could be the case for species like H. contaminatus, in the understory these insectivore bird species forage, Piculus aurulentus and Strix hylophila. because microhabitats in the understory should differ in Climate change could also be a contributing factor their response towards fragmentation. to the decline of bird species with a more southern The extinction pattern found for P EMG follows distributional range. Changes in temperature and a widespread global pattern in tropical fragmented precipitation levels can have direct and indirect effects on landscapes, with higher extinction risk and/or declines bird populations (Crick 2004). Direct effects consist, for in insectivores and large frugivores (reviewed in Bregman example, in shifts in the reproduction period of several bird et al. 2014). However, other guilds like sub-canopy and species (Crick 2004), while indirect effects are changes in canopy omnivores were susceptible to local extinction bird resources like plants and insects (Bale et al. 2002), or decline in PEMG, a pattern of species loss that does particularly those with restricted climatic ranges or adapted not conform to the usual widespread pattern of global to lower temperatures (Butterfield & Coulson 1997). species loss in tropical fragmented landscapes (Bregman Therefore, birds as well as plants and insects associated et al. 2014). Extinctions or decline in other guilds that to colder habitats (as Araucaria Forest) could have are usually not affected by fragmentation could be related declined in PEMG due to the elevation of temperatures to particularities of the area in question, such as history, in this region (Walther et al. 2002). For example, H. time of isolation, connectivity with other forest areas and contaminatus has a specialized bill (Whitney & Pacheco surrounding matrix (Sigel et al. 2010). 1994) and a foraging strategy that involves searching Revista Brasileira de Ornitologia, 24(3), 2016 Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. arthropods in substrates (e.g. moss and lichen) that are Data limitations more common in colder regions (Parrini et al. 2009). There is little information on the avifauna of northern Colonizations Paraná state before the colonization and expansion of human activities. For instance, naturalists did not visit the th Birds species with a more northern distributional range region close to the municipality of Londrina in the 19 made up the majority of the 11 colonizing species. century. However, Peter W. Wetscot in the 1930s made For example, N. ocellatus, Amazilia lactea, Myiarchus an important account about the capture of a single Harpy tyrannulus, M. flaveo la, and Thlypopsis sor dida. Some Eagle (Harpia harpyja) individual near the municipality of these species are clearly associated with open areas, of Londrina (Scherer-Neto & Straube 1995). This like Cerrado (e.g. M. tyrannulus and M. flaveo la) (Sick record suggests that the avifauna in northern Paraná was 1997). The elevation of temperature in the region in the originally much richer in species number. Some groups, last decades (Walther et al. 2002), together with forest like great raptors (Accipitridae, e.g. Spizaetus ornatus), fragmentation that generates more open habitats for were never recorded in PEMG or the region, and their species typical of Cerrado, could explain why bird species presence can only be inferred by the use of distributional with a more northern distributional range and of drier maps. This indicates that the avifauna present in P EMG, habitats are expanding into this more moist region. An as well as the number of species locally extinct, could in emblematic case is M. flaveo la, considered a threatened fact be underestimated because of the lack of information species in Paraná, which used to have only a few records in on species distributions prior to the creation of the reserve the north of the state (Mikich & Bérnils 2004) but seems (Lees & Pimm 2015). to be currently expanding to novel areas (see WikiAves. The “indeterminate” species (species with few and com.br for current records in Paraná state). infrequent records), which were recorded only in the first The guilds with t he highest number of species years of monitoring could in fact have been common in to have colonized PEMG were edge insectivores, edge the past, but our time frame captured the presence of omnivorous, nectarivores and nocturnal insectivores. Bird these species when they were at the end of their decline. species from these guilds are mainly associated with more For example, records of Sclerurus scansor and the “Near open areas. PEMG is inserted in a fragmented landscape threatened” Phylloscartes sylviolus and P. paulista could where edge effect is favored, which could explain why have been the last ones in PEMG. The maintenance of guilds associated with open habitats were the ones with bird monitoring in PEMG can provide more information the highest number of colonizing species (Thiollay 1992, to assess the local status of such species in the future. Franz et al. 2010). To reinforce this point, as mentioned Future bird monitoring in PEMG should adopt a above, in the beginning of 2000 there was a deforestation standardized method so that different time periods can of the buffer zone, which probably increased e dge effect be appropriately compared. For example, if point counts in one of the most preserved areas of the reserve. in PEMG had a standardized protocol (e.g. the same Two carnivore species, Buteo brachyurus and Leptodon location, sampling time and radius of detection), we cayanensis, were considered as colonizers according to our would have been able to use multivariate methods such criteria. These species can be easily detected in the field as NMDS to compare bird abundance and composition because they constantly vocalize (mainly in the breeding along different time periods. We argue that it is important season) and are commonly found on thermals with to sample the same points and use the same sampling vultures (Ferguson-Lees & Christie 2001, G. Willrich, procedures used in 2014. The reason is the number of pers. obs.). This fact indicates that their absence before trails used and because points are distributed both in 2005 is not a consequence of under-sampling, but could the plateau and in the altitudinal gradient of the reserve. be a possible turnover of predators in PEMG. Forest We also advocate for the increase in the use of mist net fragmentation can lead to changes in the composition and ringing, as initiated in 2015, so that population sizes of raptors without an actual change in the number of could be estimated for several species over the years. The raptor species (Jullien & Thiollay 1996). Thus, habitat evaluation of the data obtained by these methodologies loss (promoted by agriculture expansion in the region) will allow a better comprehension of species declining together with hunting activities, both of which are tendencies in the future. considered to be the main threats to populations of large raptors (Thiollay 1985, Bildstein et al. 1998, ICMBio Implications for protected areas 2008), could have gradually eliminated large raptors from the landscape, favouring smaller raptors species that can The dynamism encountered for this bird community over tolerate more fragmented habitats, such as the species the years was weak, which indicates that most bird species mentioned above. were able to persist/occupy PEMG after it was declared a Revista Brasileira de Ornitologia, 24(3), 2016 Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. P. & Carvalho, J. 2011. Bird species abundance-occupancy legal reserve. If we consider the avifauna list of Scherer- patterns and sensitivity to forest fragmentation: implications Neto et al. (2011), PEMG harbors almost 45% of all for conservation in the Brazilian Atlantic Forest. Biological bird species present in Paraná state, and together with the Conservation, 144: 2213–2222. small species dynamism over the years, the role of PEMG Anjos, L.; Collins, C. D.; Holt, R. D.; Volpato, G. H.; Lopes, E. for the conservation of biodiversity in northern Paraná V.; Bochio, G. M. 2015. Can habitat specialization patterns of Neotropical birds highlight vulnerable areas for conservation in is undeniable. Like many other protected areas, PEMG the Atlantic Rainforest, southern Brazil? Biological Conservation, is under constant pressure. For example, a recent plan to 188: 32–40. build an airport in the vicinity of PEMG was rejected due Anjos, L. & Ferreira, A. R. J. 1998. Registros de campo de Hylocharis to the efforts of the Instituto Ambiental do Paraná (IAP) sapphirina e H. cyanus na região de Londrina, norte do Estado do Paraná, sul do Brasil (Trochiliformes: Trochilidae).  Revista and a local NGO (MAE). However, other development Brasileira de Ornitologia, 6: 51. projects such as the implementation of industries next to Anjos, L.; Holt, R. D. & Robinson, S. 2010. Position in the PEMG are still under discussion. distributional range and sensitivity to forest fragmentation Furthermore, in a new concept of conservation called in birds: a case history from the Atlantic Forest, Brazil. Bird Conservation International, 20: 392–399. “biodiversity-friendly landscapes”, which aims to create a Anjos, L. & Schuchmann, K. L. 1997. Biogeographical affinities of more functional and connected landscape that conciliates the avifauna of the Tibagi River Basin, Parana drainage system, human necessities and biodiversity conservation (Melo et southern Brazil. Ecotropica, 3: 43–65. al. 2013), PEMG could act as a source for many bird Anjos, L.; Schuchmann, K. L. & Berndt, R. 1997. Avifaunal populations that could expand to surrounding areas composition, species richness and status in the Tibagi River Basin, Parana state, southern Brazil. Ornitología Neotropical, 8: 145–173. of less preserved forest fragments or new restoration Anjos, L.; Volpato, G. H.; Lopes, E. V.; Serafini, P. P.; Poletto, F . areas (Brancalion et al. 2013). Together with the use of & Aleixo, A. 2007. The importance of riparian forest for the ecological corridors and restoration areas that increase maintenance of bird species richness in an Atlantic Forest remnant, connectivity within this highly fragmented landscape, it is southern Brazil. Revista Brasileira de Zoologia, 24: 1078–1086. possible to increase rescue effects among bird populations Anjos, L.; Zanette, L. & Lopes, E. V. 2004. Effects of fragmentation on the bird guilds of the Atlantic Forest in north Paraná, southern of nearby forest fragments, thus increasing the chances of Brazil. Ornitología Neotropical, 15: 137–144. maintaining current biodiversity in the long run. Bale, J.; Masters, G. J.; Hodkinson, I. D.; Awmack, C.; Bezemer, T. M.; Brown, V. K.; Butterfield, J.; Buse, A.; Coulson, J. C.; Farrar, J.; Good, J. E. G.; Harrington, R.; Hartley, S.; Jones, T. H.; Lindroth, R. L.; Press, M. C.; Symrnioudis, I.; Watt, A. ACKNOWLEDGEMENTS D. & Whittaker, J. B. 2002. Herbivory in global climate change research: direct effects of rising temperature on insects herbivores. CAPES provided scholarships to G. Willrich, L. C. Global Change Biology, 8: 1–16. Calsavara, G. M. Bochio and G. L. M. Rosa. L. dos Anjos Bencke, G. A.; Mauricio, G. N.; Develey, P. F. & Goerk, J. M. (eds.). received a grant form CNPq (306293/2014-5) during 2006. Áreas importantes para a conservação das aves no Brasil: Parte 1 - Estados do domínio da Mata Atlântica. São Paulo: SAVE Brasil. the development of this study. IAP, ICMBio and IBAMA Bernarde, P. S. & Anjos, L. 1999. Distribuição espacial e temporal provided research licenses (IAP No. 33.14 and No. 40.14; da anurofauna no Parque Estadual da Mata dos Godoy, Londrina, SISBIO No. 45092-1; IBAMA/CEMAVE No. 3892/1) Paraná, Brasil (Amphibia: Anura). Comunicação do Museu de for bird monitoring and logistic support was provided by Ciências e Tecnologia da PUCRS, Série Zoologia, 12: 127–140. Bernarde, P. S & Machado, R. A. 2006. Répteis Squamata do Parque PEMG employees. We would also like to thank Edson Estadual Mata dos Godoy, p. 114–120. In: Torezan, J. M. D. (ed.). Mendes Francisco and Rafael Campos de Barros for Ecologia do Parque Estadual Mata dos Godoy. Londrina: Itedes. helping during fieldwork in 2014. We also thank the Bibby, C. J.; Burgess, N. D. & Hill, D. A. 1993. 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Nomenclature of species follows Piacentini et al. (2015) and endemic species (E) of Atlantic Forest follows Bencke et al. (2006). Literature review and unpublished data before 2005 (in parenthesis the period of sampling): 1) Anjos et al. 1997 (1993–1996); 2) Anjos & Ferreira 1998 (1997); 3) Anjos 2001 (1996); 4) Anjos et al. 2004 (1997); 5) Anjos field works (1993, 1995–1999); 6) Anjos field works (2001–2002); 7) Anjos et al. 2007 (2001); 8) Lopes et al. 2006 (2003–2004); 9) Anjos et al. 2011 and unpublished data (2004–2005). Literature review and unpublished data after 2005 (in parenthesis the period of sampling): 10) Santana & Anjos 2010 (2007); 11) Bochio & Anjos 2012 (2009–2010); 12) Bochio field works (2009–2010); 13) O liveira field works (2009–2015); 14) Muzi field works (2010–2012); 15) Zaiden et al. 2015 (2011); 16) Rosa field works (2009– 2015); 17) Calsavara field works (2013–2015); Willrich field works (2014–2015); Mist nets (2015). Local Status: FP – forest persistent; NFP – non-forest persistent; D – forest persistent and declining; PE – possibly extinct; EX – extinct; FM – frequent migrant; OF – occasional migrant; C – colonizer; S – sporadic species; I – indeterminate. Conservation Status: VU – vulnerable; EN – endangered; CR – critically endangered; NT – near threatened; DD – data deficient; PR – regional level (Mikich & Bérnils 2004); BR – national level (ICMBio 2014); GL – global level (IUCN 2015). Guilds: CA – carnivores; CE – carrion eaters; LF – large frugivores; SF – small frugivores; SE – seedeaters; NE – nectarivores; GI – ground insectivores; UI – understory insectivores; TI – trunk and twig insectivores; SCI – sub-canopy and canopy insectivores; AI – aerial insectivores; EI – edge insectivores; NI – nocturnal insectivores; GO – ground omnivores; UO – understory omnivores; SCO – sub-canopy and canopy omnivores; EO – edge omnivores; AO – aquatic omnivores and PI – piscivorous. Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Tinamidade                              Tinamus solitarius (Vieillot, 1819) E X   XXXXX   X             PE NT-GL; VU-PR GO Crypturellus obsoletus (Temminck, 1815) X   XXXXX   X   XXXX   X   X   FP   GO Crypturellus undulatus (Temminck, 1815) X   X   X                   EX CR-PR GO Crypturellus parvirostris (Wagler, 1827) X  X  X  X  X   X X X    X  X  FP   GO Crypturellus tataupa (Temminck, 1815) X   XXX   X   X   XXXX   XXX   FP   GO Rhynchotus rufescens (Temminck, 1815)                 X    X   X   S   GO Nothura maculosa (Temminck, 1815) X                X X     X   NFP   GO Anatidae                              Dendrocygna viduata (Linnaeus, 1766) X                       S   AO Cracidae                              Penelope superciliaris Temminck, 1815 X   XXXXX   X   XXXXXXXX   FP   LF Aburria jacutinga (Spix, 1825) E X   X                     EX EN-GL; EN-BR; EN-PR LF Crax fasciolata Spix, 1825 X   X                     EX VU-GL; CR-PR LF Odontophoridae                              Odontophorus capueira (Spix, 1825) E X                       EX   GO Ardeidae                              Nycticorax nycticorax (Linnaeus, 1758)                 X      X   S   AO Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Butorides striata (Linnaeus, 1758)                 X        S   AO Bubulcus ibis (Linnaeus, 1758 X                     X   S   GO Ardea cocoi Linnaeus, 1766                    X     S   AO Ardea alba Linnaeus, 1758                    X     S   AO Syrigma sibilatrix (Temminck, 1824)                      X   S   GO Egretta thula (Molina, 1782)                    X     S   AO Threskiornithidae                              Mesembrinibis cayennensis (Gmelin, 1789)                      X   S NT-PR AO Theristicus caudatus (Boddaert, 1783)                 X        S   GO Cathartidae                              Cathartes aura (Linnaeus, 1758) X                X    X   X   FP   CE Coragyps atratus (Bechstein, 1793) X                X    X X X   FP   CE Sarcoramphus papa (Linnaeus, 1758) X                   X X X   FP   CE Accipitridae                              Leptodon cayanensis (Latham, 1790)                 X      X   C   CA Elanoides forficatus (Linnaeus, 1758) X                X    X   X   FM   AI Elanus leucurus (Vieillot, 1818) X                X    X     NFP   CA Harpagus diodon (Temminck, 1823) X                       OM   CA Accipiter striatus Vieillot, 1808 X       X          X        FP   CA Ictinia plumbea (Gmelin, 1788) X     X X X   X      X    X   X   FM   AI Heterospizias meridionalis (Latham, 1790)                      X   S   CA Rupornis magnirostris (Gmelin, 1788) X       X   X      X    X X X   FP   CA Geranoaetus albicaudatus (Vieillot, 1816)                 X        S   CA Buteo nitidus (Latham, 1790) X                       I   CA Buteo brachyurus Vieillot, 1816                 X X     X   C   CA Aramidae                               Aramus guarauna (Linnaeus, 1766)                       X   S   AO Rallidae                              Aramides saracura (Spix, 1825) E X     X   X   X   X X X      X   FP   GI Laterallus melanophaius (Vieillot, 1819) X                       I   GI Pardirallus nigricans (Vieillot, 1819)                      X   I   GI Charadriidae                              Vanellus chilensis (Molina, 1782) X                X    X   X   NFP   GI Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Columbidae                              Columbina talpacoti (Temminck, 1810) X                X    X X X   FP   SE Columbina squammata (Lesson, 1831) X                X    X     FP   SE Columbina picui (Temminck, 1813) X                X    X   X   NFP   SE Claravis pretiosa (Ferrari-Perez, 1886) X       X   X   X X    X    X   FP   LF Patagioenas picazuro (Temminck, 1813) X   XXXXX   X   XXX   XXXX   FP   EO Patagioenas cayennensis (Bonnaterre, 1792) X   XXXXX   X   XXX   XX   X   FP   LF Patagioenas plumbea (Vieillot, 1818) X   X                X      D   LF Zenaida auriculata (Des Murs, 1847) X                X    X X X   NFP   EO Leptotila verreauxi Bonaparte, 1855 X   XXXXX   X   XXXXXXXX   FP   LF Leptotila rufaxilla (Richard & Bernard, 1792) X   XXX   X   X   XXXXXX   X   FP   LF Geotrygon montana (Linnaeus, 1758) X   XXXXX   X   XXXXXX   X   FP   LF Cuculidae                              Piaya cayana (Linnaeus, 1766) X   XXXXX   X   XXXX   XXX   FP   SCI Coccyzus melacoryphus Vieillot, 1817 X    X      X   X X X      X   FM   EI Coccyzus americanus (Linnaeus, 1758) X    X   X X   X             OM   SCO Coccyzus euleri Cabanis, 1873 X      X X                 OM DD-PR SCI Crotophaga ani Linnaeus, 1758 X   X              X    X   X   NFP   EI Guira guira (Gmelin, 1788) X                X    X X X   NFP   EI Tapera naevia (Linnaeus, 1766) X       XX         XX   X   XXX   FP   EI Dromococcyx pavoninus Pelzeln, 1870 X         X   XXXX   X   X   FP   UI Tytonidae                              Tyto furcata (Temminck, 1827) X                X    X   X   FP   CA Strigidae                              Megascops choliba (Vieillot, 1817) X       X          X X   X   X   FP   NI Pulsatrix perspicillata (Latham, 1790) X   X   X                   EX VU-BR; DD-PR CA Pulsatrix koeniswaldiana (Bertoni & Bertoni, 1901) E X   XXXX             X     X   X   FP   CA Bubo virginanus (Gmelin, 1788) X                       S   CA Strix hylophila Temminck, 1825 E X   X   X               X     D NT-GL CA Strix virgata (Cassin, 1849)                      X   I DD-PR CA Glacidium brasilianum (Gmelin, 1788) X  X X X  X  X       X    X  X  FP   NI Athene cunicularia (Molina, 1782) X                X    X   X   NFP   NI Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Th Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Nyctibiidae                              Nyctibius aethereus (Wied, 1820) X                       I EN-BR; DD-PR NI Nyctibius griseus (Gmelin, 1789) X                X    X   X   FP   NI Caprimulgidae                              Nyctiphrynus ocellatus (Tschudi, 1844)                 X    X   X   C EN-PR NI Antrostomus rufus (Boddaert, 1783) X                   X     FP   NI Lurocalis semitorquatus (Gmelin, 1789) X   X              X      X   FM   NI Nyctidromus albicollis (Gmelin, 1789) X               X X    X   X   FP   NI Hydropsalis parvula (Gould, 1837)                    X   X   C   NI Hydropsalis torquata (Gmelin, 1789)                 X        S   NI Podager nacunda (Vieillot, 1817) X                X      X   FM   NI Chordeiles minor (Forster, 1771) X                       OM DD-PR NI Chordeiles acutipennis (Hermann, 1783) X                       OM   NI Apodidae                              Cypseloides fumigatus (Streubel, 1848)                 X        S   AI Streptoprocne zonaris (Shaw, 1796) X                X        S   AI Chaetura cinereiventris Sclater, 1862 X                     X   OM   AI Chaetura meridionalis Hellmayr, 1907 X                X    X   X   FM   AI Trochilidae                              Phaethornis squalidus (Temminck, 1822) E                 X        I   NE Phaethornis pretrei (Lesson & Delattre, 1839) X                X        FP   NE Phaethornis eurynome (Lesson, 1832) E X  X  X X X  X       X X  X  X  FP   NE Eupetomena macroura (Gmelin, 1788) X                X    X X    FP   NE Florisuga fusca (Vieillot, 1817) E X                     X   FP   NE Colibri serrirostris(Vieillot, 1816) X                       I   NE Anthracothorax nigricollis (Vieillot, 1817) X   X X             X    X     FP   NE Stephanoxis lalandi (Vieillot, 1818) E X                   X     I   NE Chlorostilbon lucidus (Shaw, 1812) X    X    X   X      X X     X   FP   NE alur ania glaucopis (Gmelin, 1788) E X     XXXX   X       XX       X   FP   NE Hylocharis sapphirina (Gmelin, 1788) X                       I   NE Hylocharis cyanus (Vieillot, 1818)   X                      I   NE Hylocharis chrysura (Shaw, 1812) X                X X   X   X   FP   NE Leucochloris albicollis (Vieillot, 1818) E X                X        OM   NE Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Amazilia versicolor (Vieillot, 1818)                 X X     X   C   NE Amazilia fimbriata (Gmelin, 1788) X                   X   X   FP   NE Amazilia lactea (Lesson, 1832)                 X X   X     C   NE Trogonidae                             Trogon surrucura Vieillot, 1817 E X   XXXXX   X   XXXXXXXX   FP   SCO Trogon rufus Gmelin, 1788 X   XXXXX   X   XXXXXXXX   FP   SCO Alcedinidae                             Megaceryle torquata (Linnaeus, 1766)                      X   I   PI Chloroceryle amazona (Latham, 1790)                      X   I   PI Momotidae                              Baryphthengus ruficapillus (Vieillot, 1818) E X   XXXXX   X   XXXXXXXXX FP   UI Galbulidae                              Galbula ruficauda Cuvier, 1816 X                       I NT-PR EI Bucconidae                             Notharchus swainsoni (Gray, 1846) E X   X              X      X   FP   SCO Nystalus chacuru(Vieillot, 1816) X                       S   EO Nonnula rubecula (Spix, 1824) X     X     X       XXXX   XXXX FP   UI Ramphastidae                              Ramphastos dicolorus Linnaeus, 1766 E X   XXX   X   X   XXXXXXXX   FP   SCO Selenidera maculirostris (Lichtenstein, 1823) E X   XXXXX   X   XXXXXXXX   FP   SCO Pteroglossus bailloni (Vieillot, 1819) E X   X   X   X       XXXXX     X   FP NT-GL SCO Pteroglossus aracari (Linnaeus, 1758) X   XXXXX       X     X       D VU-PR SCO Pteroglossus castanotis Gould, 1834                    X   X   I   SCO Picidae                             Picumnus cirratus Temminck, 1825              X    X       I   TI Picumnus temminckii Lafresnaye, 1845 E X   XXXXX   X       XX   XXX   FP   TI Picumnus nebulosus Sundevall, 1866 X                       I NT-GL TI Melanerpes candidus (Otto, 1796) X                X    X X X   FP   TI Melanerpes flavifrons (Vieillot, 1818) E X   XXXXX   X   XXXX   XXX   FP   TI Veniliornis spilogaster (Wagler, 1827) E X   XXXXX   X   XXXX       X   FP   TI Piculus aurulentus (Temminck, 1821) E X    X X X           X        D NT-GL TI Colaptes melanochloros (Gmelin, 1788) X   XXXX         XXXX   X   X   NFP   TI Colaptes campestris (Vieillot, 1818) X                X    X   X   FP   TI Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Th Th Th Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Celeus flavescens (Gmelin, 1788) X   XXX           XX   X   XXX   FP   TI Dryocopus lineatus (Linnaeus, 1766) X   XXXXX   X   XXXX   X   X   FP   TI Campephiluss robustus (Lichtenstein, 1818) E X    X X          X X X    X  X  FP   TI Campephilus melanoleucos (Gmelin, 1788)     XXXX                   PE   TI Falconidae                              Caracara plancus (Miller, 1777) X       X       X X X    X   X   NFP   CA Milvago chimachima (Vieillot, 1816) X                X    X   X   NFP   CA Herpetotheres cachinnans (Linnaeus, 1758) X   XXXXX   X          X   X   FP   CA Micrastur ruficollis (Vieillot, 1817) X  X  X X X          X    X  X  FP   CA Micrastur semitorquatus (Vieillot, 1817) X   XXXXX   X   XXXX   XXX   FP   CA Falco sparverius Linnaeus, 1758 X                X    X   X   NFP   AI Falco femoralis Temminck, 1822 X                X        NFP   CA Falco peregrinus Tunstall, 1771                 X      X   OM   CA Psittacidae                             Primolius maracana (Vieillot, 1816) X     XXXX       X       X      D NT-GL; EN-PR LF Psittacara leucophthalmus (Statius Muller, 1776) X   XXXXX   X   XXXXXXXX   FP   LF Aratinga auricapillus (Kuhl, 1820) X   X   XXX   X   XXXXXXXX   FP NT-GL LF Eupsittula aurea (Gmelin, 1788) X                       S   LF Pyrrhura frontalis (Vieillot, 1817) E X   XXXXX   X   XXXXXXXX   FP   LF Forpus xanthopterygius (Spix, 1824) X  X  X              X    X  X  FP   EO Brotogeris tirica (Gmelin, 1788) E X  X  X X X  X   X X X  X X  X  FP   LF Pionopsitta pileata (Scopoli, 1769) E X   XXXXX   X   XXX   XX   X   FP   LF Pionus maximiliani (Kuhl, 1820) X   XXXXX   X   XXXXXXXX   FP   LF Amazona aestiva (Linnaeus, 1758) X   XXXXX   X   XXXXXX   X   FP   LF Triclaria malachitacea (Spix, 1824) E X   XXXXX       X       X      D NT-GL; VU-PR LF Thamnophilidae                              Dysithamnus mentalis (Temminck, 1823) X   XXXXXX X   XXXX   X   XX FP   UI Herpsilochmus rufimarginatus (Te mminck, 1822) X   XXXXXX X   XXX     X   X   FP   SCI amnophilus doliatus (Linnaeus, 1764) X      X           X    X     FP   EI amnophilus ruficapillus Vieillot, 1816 X                X    X   X   NFP   EI amnophilus caerulescens Vieillot, 1816 X   XXXXXX X   XXX     X   X   FP   UI Hypoedaleus guttatus (Vieillot, 1816) E X   XXXXXX X   XXXX   XXX   FP   SCI Mackenziaena leachii (Such, 1825) E       X X   X             I   UI Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Mackenziaena severa (Lichtenstein, 1823) E X     XXXXX X X XXXX   X   X   FP   UI Pyriglena leucoptera (Vieillot, 1818) E X   XXXXXX X X XXXX   XXXX FP   UI Drymophila rubricollis (Bertoni, 1901) E X    X    X     X    X      X   FP   UI Drymophila malura (Temminck, 1825) E X   X X X   X     X    X        FP   UI Conopophagidae                              Conopophaga lineata (Wied, 1831) E X   XXXXX   X X XXX     XXXX FP   UI Grallariidae                              Grallaria varia (Boddaert, 1783) X   X X X   X   X      X        D   GI Hylopezus nattereri (Pinto, 1937) E        X     X    X        D   GI Rhinocryptidae                              Eleoscytalopus indigoticus (Wied, 1831) E X   XXX   X       XXXX     XX   FP   UI Psilorhamphus guttatus (Ménétriès, 1835) E X   X X X   X          X      X   FP NT-PR UI Formicariidae                              Chamaeza campanisona (Lichtenstein, 1823) X   XXXXX   X   XXX      X   FP   GI Chamaeza ruficauda (Cabanis & Heine, 1859) E X                       EX   GI Scleruridae                              Sclerurus scansor (Ménétriès, 1835) E X   X                     I   GI Dendrocolaptidae                             Dendrocincla turdina (Lichtenstein, 1820) E X   XXXXX   X   XXXX   XXXX FP   TI Sittasomus griseicapillus (Vieillot, 1818) X   XXXXX   X   XXXX   XXXX FP   TI Xiphorhynchus fuscus (Vieillot, 1818) E X   XXXXX   X   XXXX   X   XX FP   TI Campylorhamphus falcularius (Vieillot, 1822) E        X       XXXX   X   X   FP   TI Lepidocolaptes angustirostris (Vieillot, 1818)       XXXX               X   S NT-PR TI Dendrocolaptes platyrostris Spix, 1825 X   XXXXX   X   XXXX   X   X   FP   TI Xiphocolaptes albicollis (Vieillot, 1818) X   XXXXX   X   XXXX   X   X   FP   TI Xenopidae                              Xenops rutilans Temminck, 1821 X   XXXXX   X   XXXX   XXX   FP   TI Furnariidae                             Furnarius rufus (Gmelin, 1788) X                X    X   X   NFP   EO Lochmias nematura (Lichtenstein, 1823)        X          X    X   X   FP   UI Clibanornis dendrocolaptoides (Pelzeln, 1859)E    X                     I NT-GL UI Automolus leucophthalmus (Wied, 1821) E X   X   X   X   X X XXXX   XXXX FP   UI Anabacerthia lichtensteini (Cabanis & Heine, 1859) E     XXXXX   X   XXXX   X   X   FP   SCI Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Philydor rufum (Vieillot, 1818) X   XXXXX   X       XX   XXX   FP   SCI Heliobletus contaminatus Pelzeln, 1859 E X   X   X X X     X           D   SCI Syndactyla rufosuperciliata (Lafresnaye, 1832) X  X  X      X       X    X  X  FP   UI Synallaxis ruficapilla Vieillot, 1819 E X   XXXXX   X X XXXX   XXXX FP   UI Synallaxis cinerascens Temminck, 1823 X   XXX   X     X XXXX   XXX   FP   UI Synallaxis frontalis Pelzeln, 1859 X   X   X           XXX     XXX   NFP   EI Synallaxis spixi Sclater, 1856 X   XXX           XXX     X   X   NFP   EI Cranioleuca obsoleta (Reichenbach, 1853) E     XXXXX   X X XXX      X   FP   TI Pipridae                              Pipra fasciicauda Hellmayr, 1906 X   X   X   X       XXXX       FP   SF Manacus manacus (Linnaeus, 1766) X   X   X                   EX   SF Chiroxiphia caudata (Shaw & Nodder, 1793) E X   XXXXX   X   XXXX   XXXX FP   SF Oxyruncidae                              Oxyruncus cristatus Swainson, 1821 X   X X X         X X         D   SCO Onychorhynchidae                             Myiobius barbatus (Gmelin, 1789) X                       I   UI Tityridae                              Schiffornis virescens (Lafresnaye, 1838) E X     X         X X X    X     FP   UO Tityra inquisitor (Lichtenstein, 1823) X   X   X   X   X   XXXX   X       FP   LF Tityra cayana (Linnaeus, 1766) X   XXXXX   X   XXXX   X   X   FP   LF Pachyramphus viridis (Vieillot, 1816) X   X              X    X     FM   SCI Pachyramphus castaneus (Jardine & Selby, 1827) X   XXXXX   X       X     X   X   FP   SCI Pachyramphus polychopterus (Vieillot, 1818) X      X X       XXXX   X   X   FM   SCI Pachyramphus validus (Lichtenstein, 1823) X  X  X X X          X X  X  X  FM   SCI Contigidae                             Phibalura flavirostris Vieillot, 1816 X                       I NT-GL; NT-PR SCO Pyroderus scutatus (Shaw, 1792) E                  X       I NT-PR LF Lipaugus lanioides (Lesson, 1844) E X                       EX NT-GL; NT-PR LF Procnias nudicollis (Vieillot, 1817) E      X                   EX VU-GL LF Pipritidae                              Piprites chloris (Temminck, 1822) X   X X X   X                 PE   SCI Platyrinchidae                              Platyrinchus mystaceus Vieillot, 1818 X     XX   X   X X XXXX   XXXX FP   UI Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Rhynchocyclidae                              Mionectes rufiventris Cabanis, 1846 E X   XXXXX           X        FP   UO Leptopogon amaurocephalus Tschudi, 1846 X   XXXXX   X   XXXX   XXX   FP   UI Corythopis delalandi (Lesson, 1830) X       X   X X XXXX   XXXX FP   UI Phylloscartes eximius (Temminck, 1822) E X   X   X                   EX NT-GL SCI Phylloscartes ventralis (Temminck, 1824) X   XXXXX       XX       XX     FP   SCI Phylloscartes paulista Ihering & Ihering, 1907 E X I NT-GL; NT-PR SCI Phylloscartes sylviolus (Cabanis & Heine, 1859) E X                       I NT-GL; DD-PR SCI Tolmomyias sulphurescens (Spix, 1825) X   XXXXX   X   XXXX   XXX   FP   SCI Todirostrum cinereum (Linnaeus, 1766) X       X          X    X   X   FP   EI Poecilotriccus plumbeiceps (Lafresnaye, 1846) X   XXXXX     X     X     X   X   FP   UI Myiornis auricularis (Vieillot, 1818) E X   XXXXX   X X     X     XXX   FP   SCI Hemitriccus diops (Temminck, 1822) E        X     X    X    X   X   FP   UI Hemitriccus obsoletus (Miranda-Ribeiro, 1906) E X       X       X X X        FP DD-PR UI Hemitriccus margaritaceiventer (d'Orbigny & Lafresnaye, 1837) X                   X     S   EI Tyrannidae                              Hirundinea ferruginea (Gmelin, 1788)                 X        S   EI Euscarthmus meloryphus Wied, 1831 X                     X   S   EI Tyranniscus burmeisteri (Cabanis & Heine, 1859) X     X     X   X X       X   FP DD-PR SCI Camptostoma obsoletum (Temminck, 1824) X   XXXXX   X   XXX     X   X   FP   SCO Elaenia flavo gaster (Thunberg, 1822) X                X      X   FP   EO Elaenia parvirostris Pelzeln, 1868 X                X X   X   X   FM   EO Elaenia mesoleuca (Deppe, 1830) X   X     X             X     FM   EO Elaenia chiriquensis Lawrence, 1865                      X   OM   EO Elaenia obscura (d'Orbigny & Lafresnaye, 1837)                      X   I   EO Myiopagis caniceps (Swainson, 1835) X   XXXXX   X   XXXX   X   X   FP   SCI Myiopagis viridicata (Vieillot, 1817) X   X              X    X   X   FP   SCI Capsiempis flaveo la (Lichtenstein, 1823) X  X X X  X    X     X    X  X  FP   UI Phyllomyias virescens (Temminck, 1824) E                      X   I   SCI Serpophaga subcristata (Vieillot, 1817) X                X    X   X   NFP   EI Legatus leucophaius (Vieillot, 1818)              XXXX   X   X   FM   SCI Myiarchus swainsoni Cabanis & Heine, 1859 X       XXX   X     XX     X   X   FM   SCI Myiarchus ferox (Gmelin, 1789)                 X    X   X   C   EI Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Myiarchus tyrannulus (Statius Muller, 1776)                 X    X   X   C   EI Sirystes sibilator (Vieillot, 1818) X   XXXXX   X   XXXX   XXX   FP   SCI Pitangus sulphuratus (Linnaeus, 1766) X  X  X  X  X   X X X    X  X  FP   EO Machetornis rixosa (Vieillot, 1819) X                X    X   X   NFP   EI Myiodynastes maculatus (Statius Muller, 1776) X   XXXXX   X   XXXX   XXX   FM   EO Megarynchus pitangua (Linnaeus, 1766) X   XXXXX   X   XXXX   XXX   FP   EO Myiozetetes similis (Spix, 1825) X  X X X  X          X    X  X  FP   EO Tyrannus melancholicus Vieillot, 1819 X  X  X              X    X  X  FM   EI Tyrannus savana Daudin, 1802 X                X    X   X   FM   EO Empidonomus varius (Vieillot, 1818) X       X          X    X   X   FM   EO Colonia colonus (Vieillot, 1818) X   XXXX     X       X     X   X   FP   SCI Myiophobus fasciatus (Statius Muller, 1776) X   X X             X X   X   X   FM   EI Pyrocephalus rubinus (Boddaert, 1783) X                X    X     FM   EI Arundinicola leucocephala (Linnaeus, 1764) X                       S   EI Cnemotriccus fuscatus (Wied, 1831) X           X X X X    X   X   FM   EI Lathrotriccus euleri (Cabanis, 1868) X   X   XXX   X X XXXX   X   XX FM   UI Contopus cinereus (Spix, 1825) X                X      X   FP   SCI Knipolegus cyanirostris (Vieillot, 1818) X                     X   FP   EI Satrapa icterophrys (Vieillot, 1818) X                       S   EI Muscipipra vetula (Lichtenstein, 1823) E X                       S   SCI Vireonidae                             Cyclarhis gujanensis (Gmelin, 1789) X   XXXXX   X   XXX     XXX   FP   SCO Hylophilus poicilotis Temminck, 1822 E X       X                 PE   EI Vireo chivi (Vieillot, 1817) X       X   X      X    X   X   FM   SCO Corvidae                              Cyanocorax chrysops (Vieillot, 1818) X   XXXXX   X   XXXX   XXX   FP   EO Hirundinidae                              Pygochelidon cyanoleuca (Vieillot, 1817) X                X X   X   X   NFP   AI Alopochelidon fucata (Temminck, 1822) X                       OM   AI Stelgidopteryx ruficollis (Vieillot, 1817) X                X X   X   X   FM   AI Progne tapera (Vieillot, 1817) X                X    X   X   FM   AI Progne chalybea (Gmelin, 1789) X                X      X   FM   AI Tachycineta leucorrhoa (Vieillot, 1817) X                     X   FM   AI Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Hirundo rustica Linnaeus, 1758 X                       OM   AI Petrochelidon pyrrhonota (Vieillot, 1817) X                       OM   AI Troglodytidae                              Troglodytes musculus Naumann, 1823 X   X       X       XXX     XXX   NFP   EI Polioptilidae                              Polioptila lactea Sharpe, 1885 E X   X X X   X                 PE NT-GL; EN-PR SCI Turdidae                              Turdus leucomelas Vieillot, 1818 X   XXXXX   X   XXXX   XXXX FP   EO Turdus rufiventris Vieillot, 1818 X   X   XXX   X   XXX     XXXX FP   EO Turdus amaurochalinus Cabanis, 1850 X  X X  X X  X   X X X    X  X  FP   EO Turdus subalaris (Seebohm, 1887) E       X X         X X X   X X X   FM   UO Turdus albicollis Vieillot, 1818 X   X   X   X   X   XXXX     XXX FP   UO Mimidae                              Mimus saturninus (Lichtenstein, 1823) X                X    X   X   NFP   EO Motacillidae                              Anthus lutescens Pucheran, 1855 X                X    X   X   NFP   EO Passerellidae                              Zonotrichia capensis (Statius Muller, 1776) X       X          X    X   X   NFP   SE Ammodramus humeralis (Bosc, 1792) X                X    X   X   NFP   EO Arremon semitorquatus Swainson, 1838 E                 X        I   SE Arremon flavirostris Swainson, 1838                 X        S   SE Parulidae                              Setophaga pitiayumi (Vieillot, 1817) X   XXXXX       XXXX   XXX   FP   SCI Geothlypis aequinoctialis (Gmelin, 1789) X                X    X   X   NFP   EI Basileuterus culicivorus (Deppe, 1830) X   XXXXX   X   XXX     XXXX FP   UI Myiothlypis flaveo la Baird, 1865          X      X X   X X X   C VU-PR EI Myiothlypis leucoblephara (Vieillot, 1817) E X   XXX   X       XXX     XXXX FP   UI Icteridae                             Cacicus chrysopterus (Vigors, 1825)                 X        I   SCO Cacicus haemorrhous (Linnaeus, 1766) X   XXXXX   X   XXXX   XXX   FP   SCO Icterus pyrrhopterus (Vieillot, 1819) X                X        FP   EO Gnorimopsar chopi (Vieillot, 1819) X                       S   EO Molothrus oryzivorus (Gmelin, 1788) X                       S   EO Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Th Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Molothrus bonariensis (Gmelin, 1789) X                X    X   X   NFP   EO Sturnella superciliaris (Bonaparte, 1850) X                X    X     NFP   EO Thraupidae                              Pipraeidea melanonota (Vieillot, 1819) X     XXXX   X       XX   X   X   FP   SCO Cissopis leverianus (Gmelin, 1788) X   XXXXX           X     X   X   FP   LF Tangara seledon (Statius Muller, 1776) E X                       I   SCO Tangara sayaca (Linnaeus, 1766) X   XXXXX   X   XXX     X   X   FP   EO Tangara preciosa (Cabanis, 1850) X                X X       FP   EO Tangara cayana (Linnaeus, 1766) X                       I NT-PR EO Nemosia pileata (Boddaert, 1783) X                X    X   X    FP   SCO Conirostrum speciosum (Temminck, 1824) X   XXXXX   X   XXXX   X   X   FP   SCO Sicalis flaveo la (Linnaeus, 1766)                    X   X   S   SE Haplospiza unicolor Cabanis, 1851 E                 X      X   C   SE Hemithraupis guira (Linnaeus, 1766) X   XXXXX   X   XXXX   X   X   FP   SCO Volatinia jacarina (Linnaeus, 1766) X                X X   X   X   FM   SE Trichothraupis melanops (Vieillot, 1818) X   XXXXX   X   XXXX   XXXX FP   UO Coryphospingus cucullatus (Statius Muller, 1776) X                X X   X   X   NFP   SE Tachyphonus coronatus (Vieillot, 1822) E X   XXXXX       XXX     X   X   FP   EO Ramphocelus carbo (Pallas, 1764) X                       S   EO Tersina viridis (Illiger, 1811) X       X   X      X X   X   X   FM   SF Dacnis cayana (Linnaeus, 1766) X       X   X   XXXX   X   X   FP   SCO Coereba flaveo la (Linnaeus, 1758) X                X    X   X   FP   NE Tiaris fuliginosus (Wied, 1830) X                       EX   SE Sporophila lineola (Linnaeus, 1758)                 X        S   SE Sporophila collaris (Boddaert, 1783) X                       S   SE Sporophila caerulescens (Vieillot, 1823) X                   X   X   NFP   SE Saltator similis d'Orbigny & Lafresnaye, 1837 X   X   XXX   X   XXXX   X   XX FP   EO Saltator fuliginosus (Daudin, 1800) E X   XXXXX   X   XXX       XX   FP   LF lypopsis sor dida (d'Orbigny & Lafresnaye, 1837)                 X    X     C   EO Pyrrhocoma ruficeps (Strickland, 1844) E X      X  X          X X  X  X  FP   UI Cardinalidae                              Piranga flav a (Vieillot, 1822) X                       EX NT-PR SCO Habia rubica (Vieillot, 1819) X   XXXXX   X     XX     XXX   FP   UO Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Amaurospiza moesta (Hartlaub, 1853) E                 X        I NT-GL SE Cyanoloxia brissonii (Lichtenstein, 1823) X                       I   SE Fringillidae                              Spinus magellanicus (Vieillot, 1805) X                       S   SE Euphonia chlorotica (Linnaeus, 1766) X   XXXXX   X   XXX     XXX   FP   SF Euphonia violacea (Linnaeus, 1758) X   XXX           XXX     X   X   FP   SF Euphonia cyanocephala (Vieillot, 1818) X   X       X      X    X   X   FM   SF Euphonia pectoralis (Latham, 1801)E X    X X   X       X X         D   SF Chlorophonia cyanea (Thunberg, 1822) X                     X   I   SF Estrildidae                              Estrilda astrild (Linnaeus, 1758) X                     X   S   SE Passeridae                             Passer domesticus (Linnaeus, 1758) X                       S   EO APPENDIX II Species found in literature review and not included in the final list (Appendix I), since they were recorded only once and could represent dubious records or because their distributional ranges do not include northern Paraná state. Nomenclature of species follows Piacentini et al. (2015). Species Literature Trogon viridis Linnaeus, 1766 Anjos et al. 1997, Anjos 2001 Cyanerpes cyaneus (Linnaeus, 1766) Anjos et al. 1997 Attila rufus (Vieillot, 1819) Anjos et al. 1997 Dysithamnus stictothorax (Temminck, 1823) Anjos et al. 1997, Anjos et al. 2004 Drymophila ferruginea (Temminck, 1822) Anjos et al. 1997, Anjos et al. 2004 Hemitriccus nidipendulus (Wied, 1831) Anjos et al. 1997 Phylloscartes oustaleti (Sclater, 1887) Anjos et al. 1997 Saltatricola atricollis (Vieillot, 1817) Anjos et al. 1997 Aramides cajaneus (Statius Muller, 1776) Anjos et al. 2007 Anabacerthia amaurotis (Temminck, 1823) Anjos et al. 2007 Patagioenas maculosa (Temminck, 1813) Bochio & Anjos 2012 Cichlocolaptes leucophrus (Jardine & Selby, 1830) Bochio & Anjos 2012 Campylorhamphus trochilirostris (Lischtenstein, 1820) Bochio & Anjos 2012 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Ornithology Research Springer Journals

Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil

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Springer Journals
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Copyright © Sociedade Brasileira de Ornitologia 2016
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2178-7875
DOI
10.1007/bf03544352
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Abstract

Revista Brasileira de Ornitologia, 24(3), 235-259 ARTICLE September 2016 Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil 1,5 1 2 3 Guilherme Willrich , Larissa Corsini Calsavara , Marcos Robalinho Lima , Renan Campos de Oliveira , 1 1 4 2 Gabriela Menezes Bochio , Gabriel Lima Medina Rosa , Vanildo Cesar Muzi and Luiz dos Anjos Programa de Pós Graduação em Ciências Biológicas, Universidade Estadual de Londrina, CEP 86051-990, Londrina, PR, Brazil. Laboratório de Ornitologia e Bioacústica, Departamento de Biologia Animal e Vegetal, Universidade Estadual de Londrina, CEP 86051-990, Londrina, PR, Brazil. ONG MAE - Meio Ambiente Equilibrado, Rua Goiás, 1774, CEP 86010-465, Centro, Londrina, PR, Brazil. Rua Japuguaçu, 234, CEP 86702-236, Jardim Bela Vista, Arapongas, PR, Brazil. Corresponding author: guigawillrich@hotmail.com Received on 04 November 2015. Accepted on 11 September 2016. ABSTRACT: Human activities have modified landscapes worldwide, promoting fragmentation and isolation of forest habitats. Such landscape modifications are responsible for changes in species composition due to extinction and colonization events. Forest species dynamism is usually affected by forest fragmentation when remaining fragments are small and isolated, but forest dynamism is usually more stable when forest fragments are large and connected. In this study we verified c hanges in bird composition during 23 years of bird monitoring at the Mata dos Godoy State Park (PEMG). We aimed to evaluate the avian community dynamism of this reserve, as well as its effectiveness in protecting biodiversity in an extremely fragmented landscape. We reviewed historical records of bird species composition and checked for any possible misidentifications, updated t he list and created an annual data set of bird species occurrence. We used this list to evaluate species persistence, species loss, and colonization over the study period. Additionally, species were classified accor ding to their guilds in order to determine which species traits were associated with local extinction. A total of 331 bird species were recorded in PEMG over 23 years of monitoring, 17 of which were considered locally extinct or possibly extinct, and 11 were recent local colonizations. This indicates that bird composition in PEMG has been relatively stable over the years. However, local extinction was more likely for large frugivores and insectivores, which are guilds already known to be more susceptible to local extinction. Colonizations, in turn, were associated with guilds of more open habitats, like edge insectivores. We suggest that extinctions and colonizations are also potentially related to species distribution ranges and climate change. Although local extinctions occurred, PEMG still maintains a significant fraction of its historical avifauna and may potentially maintain source populations for many bird species, thus making it an important reserve for the north of Paraná. KEY-WORDS: avifauna, Atlantic Forest, forest fragment dynamism, Protected Area, species persistence. INTRODUCTION ha (Ribeiro et al. 2009) and surrounded by a matrix of anthropogenic habitats (e.g. plantations and urban areas) Human activities, such as food and energy production, are (Tabarelli et al. 2010). responsible for the modification of landscapes worldwide The Atlantic Forest Biome consists of several different forest formations that have suffered different deforestation (Foley et al. 2005, Sodhi & Ehrlich 2010, Haddad et al. 2015). These activities contribute to changes in climate pressures (Galindo-Leal & Câmara 2003). In the north regimes, loss of ecosystem services such as air and water of Paraná state (southern Brazil), which is comprised by quality and decrease in forest cover, all of which result in semi-deciduous forest formations, deforestation has led biodiversity loss (DeFries et al. 2004, Foley et al. 2005, to the loss of approximately 98% of the original forest cover (Torezan et al. 2005). In this landscape scenario, Zhao et al. 2006, Haddad et al. 2015). In the Atlantic Forest Biome, a biodiversity hotspot (Myers et al. 2000), however, Mata dos Godoy State Park (Parque Estadual this scenario is alarming because only 11.4% to 16% of Mata dos Godoy - PEMG) stands out as potentially the the original forest cover still remains (Ribeiro et al. 2009). most important reserve since it is the largest and most Exacerbating this situation is the fact that the majority well preserved forest fragment in the north of Paraná state (Anjos et al. 2007, 2009). Even though this reserve is of the remaining forest fragments are smaller than 50 Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. immersed in an agro-mosaic matrix, much of the regional are an important component to determine the persistence, fauna of anurans (Bernarde & Anjos 1999, Machado & colonization and/or local extinction of species. However, Bernarde 2006), reptiles (Bernarde & Machado 2006) and before using this type of data it is important to review birds (Anjos et al. 1997, Anjos 2001) are well represented the historical records of the literature to guarantee in PEMG. Also, PEMG contains 21 threatened species that the data does not contain dubious records (i.e. and 15 rare species of Angiosperms (Rossetto & Vieira misidentification). Lees et al. (2014) suggest several ways 2013), which makes PEMG an important reserve for of dealing with misidentification. For instance, one could semi-deciduous forest formations. In fact, this protected use the distributional range of the species in question area has become a regional conservation reference not only to determine if it overlaps with the dubious record, or because of its intrinsic biological value, but also because one could possibly determine if suitable habitat for of the development of several environmental educational the species occurs in the area in question, or even the programmes with local communities. possibility of a mix up between very similar species (e.g. Despite its importance for regional conservation, Drymophila ferruginea and D. rubricollis). We have two PEMG still suffers several t hreats. The biggest threat to goals for this study, the first one to present a revised PEMG is the expansion of agriculture, which has taken historical checklist for the birds of PEMG, where we place in the last seven decades, but others threats such present species occurrence data from 1993 to 2015 and as illegal hunting, invasive species and water pollution check for possible misidentifications. Our second goal is are also present (IAP 2002). At the landscape level, the to use this revised checklist to assess the potential species continuation of habitat loss has led to an increase in forest dynamism in this reserve during the last 23 years. Because fragmentation and its associated negative outcomes, such as birds are recognized as good biological indicators and edge effects and forest fragment isolation. These landscape capable of responding to primary and secondary causes modifications could have important consequences for of environmental changes (Morrison 1986, Temple & forest fragment dynamism (Laurance 2002). According to Wiens 1989, Koskimies 1989, Kushlan 1993, Piratelli et the concept of forest fragment hyperdynamism, small and al. 2008), our approach will allow us to determine how isolated areas tend to be strongly affected by the impacts of effective P EMG is for the conservation of the regional fragmentation in a short time frame and should present, biota in the north of Paraná state. for example, high species turnover (Laurance et al. 1998, Laurance et al. 2002). Conversely, large connected forest METHODS fragments tend to suffer fewer changes in the same short time frame with a weak dynamism, because it will usually harbor a higher number of persisting species (Bierregaard Study area et al. 1992, 1998, 2002, Laurance 2010). Laurance (2002) suggested that forest fragmentation tends to Mata dos Godoy State Park (23°27'S; 51°15'W, PEMG, Figure 1) is the largest and best preserved forest fragment affect the dispersion of species and individuals, leading to an increase in colonization of generalist, invasive and in northern Paraná state, south of Brazil (Anjos et al. pathogenic species, which will usually modify biological 2007). PEMG is located in Espírito Santo District, 15 km interactions (i.e. through competition). These in turn from the center of the municipality of Londrina and over will affect both species abundance and composition the Tropic of Capricorn. This reserve covers 656 ha and is mainly composed by pristine seasonal semi-deciduous (Bierregaard et al. 1992, Laurance et al. 2002, Laurance 2002, 2010). However, the effects on forest dynamism forest (Figure 1, Torezan 2002). PEMG presents a natural will depend on the duration and strength of these and variation in topography, which allows one to divide other impacts, and on the characteristics of the forest PEMG in two different regions comprised of pristine fragment (Laurance 2002, Laurance et al. 2002). At forest. One of the regions is located in the north and consists of a plateau at an altitude of approximately 600 m, the moment, it is uncertain if PEMG has maintained its biodiversity over the years. Therefore, it is crucial to while the second region is located in the south of PEMG document how species composition has changed since and consists of a hillside that ranges from 600 to 470 m PEMG became a legal reserve to assess its current and a.s.l. (Anjos et al. 2007). This difference in elevation is future role in the protection of biodiversity. Moreover, responsible for the widespread occurrence of bamboo vegetation in the southern part of PEMG, which results this will provide a better understanding of which species are more susceptible to local extinction in semi-deciduous in differences in the occurrence of bir d species between forest formations of the Atlantic Forest. these two areas (see Anjos et al. 2007, Santana & Anjos In this study we verified if the bird community of 2010). For more details on the vegetation of PEMG see PEMG has been maintained over the years after it was Silveira (2006) and Rossetto & Vieira (2013). This reserve also harbor an area of secondary forest in the southeast, an recognised as a legal reserve in 1989. Historical data sets Revista Brasileira de Ornitologia, 24(3), 2016 Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. area of open habitats (e.g. pasture or initial regeneration) review because bird data from these specific studies had in the northern portion, and a reforestation area that was already been published in one of the ten references listed implemented twenty years ago (IAP 2002; Figure 1). in Table 1. TABLE 1. Published bird occurrence data in PEMG, Paraná state, Brazil, and the respective period in which fieldwork was conducted. Published papersPeriod of field wor k Anjos et al. 1997 1992–1996 Anjos & Ferreira 1998 September 1997 Anjos 2001 January–December 1996 Anjos et al. 2004 September–December 1997 Anjos et al. 2007 September–December 2001 Lopes et al. 2006 2003–2004 Anjos et al. 2011 2004–2005 Santana & Anjos 2010 2007 Bochio & Anjos 2012 2009–2010 Zaiden et al. 2015 2010–2011 Unpublished data, in turn, consisted of different methodologies and sampling efforts that were conducted between 1993 and 2015, these methods were: ad libitum searches, point counts, and bird capture with mist nets. Ad libitum searches by different observers were conducted in the entire area of PEMG without controlling for sampling effort. Point counts (Vielliar d & Silva 1990, Bibby et al. 1993) were performed in PEMG during three different periods: (1) 1993–2002, (2) 2004–2005, and (3) 2014. For the first period, point counts were FIGURE 1. Location of Mata dos Godoy State Park (PEMG, 23°27'S; conducted in 1993, 1995–1999, 2001 and 2002. In 51°15'W) in the north of Paraná state, south of Brazil. each of these years, with the exception of 1996, five A matrix of privately owned agricultural land point counts in pristine forest were sampled twice during surrounds the northern and western borders of PEMG, spring (October). In 1996, the same point counts were while the Apertados River borders the south and a performed once a month from January to December continuous forest fragment borders the east. Considering (Anjos 2001). Point counts in all these years (including all forest fragments surrounding PEMG up to a distance 1996) were placed 100 m apart and at least 50 m away of 1 km, connected or not to PEMG, there is a mosaic from the forest edge (Figure 1). Sampling time for each of forest cover of approximately 2800 ha (Lopes et point was 20 minutes, and the radius of detection was al. 2006). PEMG is situated in the Tibagi River basin unlimited. For the second time period, point counts (IAP 2002) and according to Köppen classification, the were conducted every season in 2004 and 2005. In this climate of the region is Cfa, subtropical humid with case, six point counts along two trails were placed 200 rainy summers, average yearly temperatures of 21°C and m apart, giving a total of 12 points (Figure 1). Point average maximum and minimum temperatures of 28°C counts were sampled for 15 minutes with a detection and 16°C, respectively. radius ≤100 m (Anjos et al. 2011). Data from spring and summer from this second time period were published Data set in Anjos et al. (2011, 2015), but for the present study we have also incorporated unpublished records from The historical data set was obtained using both the autumn and winter. The thir d point count sampling scientific literature and unpublished data. From the period occurred from September to December 2014. In scientific literature, we compiled data on bird species this case, 39 point counts (with 15 min sampling time using ten scientific papers published between 1997 and and a detection radius ≤50 m) were placed along 13 2015 (Table 1). Several studies (e.g. Anjos & Schuchmann trails, each trail consisted of three point counts at 200 1997, Anjos et al. 2010) were excluded from the literature m intervals (Figure 1). Each point count was sampled Revista Brasileira de Ornitologia, 24(3), 2016 Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. four times during the sampling period. In all of the during the entire study period and for which PEMG three-time periods, bird sampling was conducted early harbor suitable habitat for the specie. For the last case in the morning and started with species vocal activity. we were unable to classify the species as persistent, Sampling ended approximately 3 h later. extinct or colonizer. Classification into forest, non-forest Mist nets were placed in six different locations in and migrant species follows Sick (1997), del Hoyo et PEMG between February and October 2015 (Figure 1), al. (2015) and our personal observations in the study with a total sampling effort of 10,332 h.m . Mist nets area. For species that were mentioned in the literature as procedures followed Roos (2010). both forest and non-forest, we used the habitat that was Bird nomenclature and systematic classification are described as preferred for the species. in accordance with the list of Brazilian birds reviewed and The Sørensen Index of Similarity (Magurran 1988) updated by the Comitê Brasileiro de Registros Ornitológicos was used to analyse variation in species composition (Piacentini et al. 2015). The conservation status of each over time. We used this index to calculate how similar species was based on IUCN (2015), ICMBio (2014) the two time periods were (before 2005 and after 2005). and Mikich & Bérnils (2004) at the global, national and The following formula was used to calculate the Sørensen regional levels, respectively. We used Bencke et al. (2006) Index of Similarity: Ss = 2j / (a + b); where j corresponds to classify species as endemic to the Atlantic Forest. to the number of species common to both periods (before 2005 and after 2005), a represents the number of species Data analysis present before 2005 and b the number of species present after 2005 (Magurran 1988). For this analysis we first The data set was organized on an annual basis and pooled the species in the categories “extinct”, “possibly bird records were divided into two larger time periods, extinct”, “forest persistent”, “non-forest persistent”, before and after 2005 (Appendix I). We only considered “forest persistent and declining” and “colonizer”. We then presence and absence data because sampling effort among excluded “colonizer” species in order to verify only the studies, from the scientific literature or unpublished data, effects of extinctions over the periods. were not standardized, making quantitative comparisons In order to evaluate if certain traits made the unfeasible. Based on this list, we carefully reviewed species more prone to extinction, species were grouped questionable records (e.g. misidentifications) in or der to according to their guilds. Species were classified using a eliminate “false presences”. This procedure allowe d for the combination of food resources explored by the species correct evaluation of local species persistence in PEMG and habitat choices, which were mainly based on Willis (Lees et al. 2014) according to the categories presented (1979), Ribon et al. (2003), Giraudo et al. (2008) and below. our own field o bservations. Species were classified as: We categorized bird species as: 1) “forest persistent”, carnivores (CA); carrion eaters (CE); large frugivores forest bird species that were recorded regularly in the (LF); small frugivores (SF); seedeaters (SE); nectarivores entire study period; 2) “non-forest persistent”, species (NE); ground insectivores (GI); understory insectivores that inhabit non-forest habitats and were recorded (UI); trunk and twig insectivores (TI); sub-canopy and regularly in the entire study period; 3) “forest persistent canopy insectivores (SCI); aerial insectivores (AI); edge and declining”, forest species that were recorded regularly insectivores (EI); nocturnal insectivores (NI); ground up to 2005, but were only recorded in one or two years omnivores (GO); understory omnivores (UO); sub- after 2005; 4) “possibly extinct”, forest species that were canopy and canopy omnivores (SCO); edge omnivores regularly recorded until 2005, but were not recorded (EO); aquatic omnivores (AO); and piscivorous (PI). thereafter; 5) “extinct”, forest species that were regularly To visualize which guilds increased or decreased in recorded until 2000, but not afterwards, or species number of species during the last 23 years in PEMG, that are easily detectable (e.g. Odontophorus capueira) we plotted a graph with the number of species in each but were recorded only in the first years of monitoring guild that were present before and after 2005. For this (1993–1996); 6) “frequent migrants”, migrant species in analysis, we excluded the following categories: “frequent the south of Brazil that were present during most of the migrant”, “occasional migrant”, “sporadic species” and studied years; 7) “occasional migrants”, migrant species “indeterminate”. We considered a species to be declining that were occasionally found during the study period; and in risk of future extinction when it presented a decline 8) “colonizer”, species that were found in consecutive in occurrence records after 2005. We used this data to years in the study area after 2005 and not before; 9) determine the future tendency in the number of species “sporadic species”, species for which PEMG harbor for each guild. Future tendency of a guild was defined as unsuitable habitat (e.g. Ardeidae) and that had few and the number of species present after 2005, subtracting the infrequent records during the entire study period; 10) number of species in the category “forest persistent and “indeterminate”, species with few and infrequent records declining” (Figure 2). Revista Brasileira de Ornitologia, 24(3), 2016 Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. considered locally extinct, five species as possibly extinct Before 2005 After 2005 and 11 species were considered to be recent colonizations, Future tendency according to our criteria (Table 2). For the remaining species, 42 species were considered migrants (30 frequent and 12 occasional) and 70 were recorded only once or twice during the monitoring period (37 classified as sporadic and 33 as indeterminate; Appendix I). A total of 28 bird species (~10%) were considered either as locally extinct, possibly extinct or persistent and declining. Moreover, of the 13 species considered threatened at global, national or regional levels recorded in PEMG during the entire monitoring period, seven are CA CE LF SF SE NE GI UI TI SCI AI EI NI GO UO SCO EO already locally extinct or possibly extinct and three others Guild are considered to be declining (Table 2). Three species FIGURE 2. Number of species before and after 2005 for each bird considered near threatened at regional and global levels guild in Mata dos Godoy State Park (PEMG), Paraná state, Brazil. Only the following categories were considered: “extinct”, “possibly were also considered locally extinct in PEMG. However, extinct”, “colonizer”, “persistent and declining” and “persistent”. two species, Myiothlypis flaveo la and Nyctiphrynus For the latter category, both forest and non-forest bird species were ocellatus, which are threatened bird species at the regional considered. Species that presented a decline in occurrence records after level, were considered to have recently colonized PEMG. 2005 were considered to be declining and in risk of future extinction and this data were used to determine the future tendency in the If we exclude the species that went locally extinct, PEMG number of species for each guild. Guild: CA – carnivores; LF – large currently harbor 319 bird species (68 endemic to Atlantic frugivores; SF – small frugivores; SE – seedeaters; NE – nectarivores; Forest), out of which eight are threatened species, 16 near GI – ground insectivores; TI – trunk and twig insectivores; SCI – threatened and five data deficient for the Paraná state sub-canopy and canopy insectivores; EI – edge insectivores; NI – (Appendix I). nocturnal insectivores; GO – ground omnivores; SCO – sub-canopy and canopy omnivores; EO – edge omnivores. The most representative guilds, considering the total number of bird species originally recorded at RESULTS PEMG (331), were edge omnivores (n = 36, 10.9%), understory insectivores (n = 31, 9.4%), sub-canopy and A total of 331 bird species were recorded during 23 years canopy insectivores (n = 30, 9.0%), edge insectivores of bird monitoring in PEMG (Appendix I). Thirteen (n = 28, 8.4%), large frugivores (n = 26, 7.8%), sub- species found in the literature review were not included canopy and canopy omnivores (n = 23, 6.9%), trunk in this list of 331 bird species, either because their ranges and twig insectivores (n = 22, 6.6%) and carnivores (n did not include northern Paraná, or because they were = 22, 6.6%) (Appendix I). In general, insectivores were recorded only once and could represent dubious records highly representative with 149 species (45.0%), followed (Appendix II). Of the 331 species with confirmed by omnivores (84, 25.4%) and frugivores (35, 10.6%). presence in PEMG, 74 species are endemic to the Atlantic The two guilds with t he highest number of species Forest, while 13 species are considered threatened either going locally extinct were large frugivores (33.3%, n = 4) at the global, national or regional levels (Appendix and ground omnivores (16.6%, n = 2) (Table 3). Possibly I). Furthermore, 19 species are considered “Near extinct species were mainly represented by sub-canopy and threatened” at global and regional levels, and five species canopy insectivores (40%, n = 2). Large frugivores had the are considered as “Data deficient” in the Paraná state. highest number of forest bird species that are declining Bird community composition before and after 2005 (27.2%, n = 3), followed by ground insectivores (18.2%, n was very similar (93%; Ss = 0.932). When colonizer = 2). Colonizers, on the other hand, were well represented species were excluded, bird species similarity between the by the insectivores and omnivores guilds (Table 3). two time periods increased (95%, Ss = 0.957), as expected. Large frugivores are expected to have a higher number Therefore, P EMG presented a stable avifauna during the of future local extinctions because of the decline in the 23 years of bird monitoring. However, the number of number of species occurrence for this category (Figure 2). species that went extinct promoted a higher dissimilarity Small frugivores, ground insectivores, ground omnivores, (5%) between the two time periods than the number of trunk and twig insectivores, as well as sub-canopy and species that later colonized PEMG (2%). This stability canopy insectivores were guilds that had a high number was expected because 191 out of the 331 species, that were of species at risk of local extinction. Conversely, edge originally found in PEMG, were considered as persistent insectivores, edge omnivores, nocturnal insectivores and (150 forest persistent, 30 non-forest persistent and 11 nectarivores tended to maintain local populations and may forest persistent and declining), while only 12 species were even see increases in the number of species in the future. Revista Brasileira de Ornitologia, 24(3), 2016 Number of species Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. TABLE 2. Species considered extinct, possibly extinct, declining and recent colonisers in PEMG, Paraná state, Brazil. Local Status: EX – extinct; PE – possibly extinct; D – forest persistent and declining; C – colonizer. Conservation Status: VU – vulnerable; EN – endangered; CR – critically endangered; NT – near threatened; DD – data deficient; PR – regional level (Mikich & Bérnils 2004); BR – national level (ICMBio 2014); GL – global level (IUCN 2015). Guild: CA – carnivores; LF – large frugivores; SF – small frugivores; SE – seedeaters; NE – nectarivores; GI – ground insectivores; TI – trunk and twig insectivores; SCI – sub-canopy and canopy insectivores; EI – edge insectivores; NI – nocturnal insectivores; GO – ground omnivores; SCO – sub-canopy and canopy omnivores; EO – edge omnivores. Endemic species (E) follows Bencke et al. (2006). Species Local status Conservation status Guild Crypturellus undulatus (Temminck, 1815) EX CR-PR GO Aburria jacutinga (Spix, 1825) EEX EN-GL; EN-BR; EN-PR LF Crax fasciolata Spix, 1825 EX VU-GL; CR-PR LF Odontophorus capueira (Spix, 1825) EEX   GO Pulsatrix perspicillata (Latham, 1790) EX VU-BR; DD-PR CA Chamaeza ruficauda (Cabanis & Heine, 1859) EE X   GI Manacus manacus (Linnaeus, 1766) EX   SF Lipaugus lanioides (Lesson, 1844) EEX NT-GL; NT-PR LF Procnias nudicollis (Vieillot, 1817) EEX VU-GL LF Phylloscartes eximius (Temminck, 1822) EEX NT-GL SCI Tiaris fuliginosus (Wied, 1830) EX   SE Piranga flav a (Vieillot, 1822) EX NT-PR SCO Tinamus solitarius (Vieillot, 1819) E PE NT-GL; VU-PR GO Campephilus melanoleucos (Gmelin, 1788) PE   TI Piprites chloris (Temminck, 1822) PE   SCI Hylophilus poicilotis Temminck, 1822 E PE   EI Polioptila lactea Sharpe, 1885 E PE NT-GL; EN-PR SCI Patagioenas plumbea (Vieillot, 1818) D   LF Strix hylophila Temminck, 1825 E D NT-GL CA Pteroglossus aracari (Linnaeus, 1758) D VU-PR SCO Piculus aurulentus (Temminck, 1821) E D NT-GL TI Primolius maracana (Vieillot, 1816) D NT-GL; EN-PR LF Triclaria malachitacea (Spix, 1824) E D NT-GL; VU-PR LF Grallaria varia (Boddaert, 1783) D   GI Hylopezus nattereri (Pinto, 1937) E D   GI Heliobletus contaminatus Berlepsch, 1885 E D   SCI Oxyruncus cristatus Swainson, 1821 D   SCO Euphonia pectoralis (Latham, 1801) E D   SF Leptodon cayanensis (Latham, 1790) C   CA Buteo brachyurus Vieillot, 1816 C   CA Nyctiphrynus ocellatus (Tschudi, 1844) C EN-PR NI Hydropsalis parvula (Gould, 1837) C   NI Amazilia versicolor (Vieillot, 1818) C   NE Amazilia lactea (Lesson, 1832) C   NE Myiarchus ferox (Gmelin, 1789) C   EI Myiarchus tyrannulus (Statius Muller, 1776) C   EI Myiothlypis flaveo la Baird, 1865 C VU-PR EI Thlypopsis sor dida (d'Orbigny & Lafresnaye, 1837) C   EO Haplospiza unicolor Cabanis, 1851 E C   SE Revista Brasileira de Ornitologia, 24(3), 2016 Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. TABLE 3. Representation of guilds (%) in each category in PEMG, Paraná state, Brazil. Each column corresponds to 100% of the respective category. Guilds are as follows: CA – carnivores; CE – carrion eaters; LF – large frugivores; SF – small frugivores; SE – seedeaters; NE – nectarivores; GI – ground insectivores; UI – understory insectivores; TI – trunk and twig insectivores; SCI – sub-canopy and canopy insectivores; AI – aerial insectivores; EI – edge insectivores; NI – nocturnal insectivores; GO – ground omnivores; UO – understory omnivores; SCO – sub-canopy and canopy omnivores; EO – edge omnivores; AO – aquatic omnivores; and PI – piscivorous. Extinct Possibly extinct Forest persistent declining Forest persistent Non-forest persistent Colonizer Guild (100% = 12) (100% = 5) (100% = 11) (100% = 150) (100% = 30) (100% = 11) CA 8.3 - 9.1 4.7 13.3 18.2 CE - - - 2.0 - - LF 33.3 - 27.2 11.3 - - SF 8.3 - 9.1 2.7 - - SE 8.3 - - 1.3 13.3 9.1 NE - - - 6.7 - 18.2 GI 8.3 - 18.2 1.3 3.3 - UI - - - 18.0 - 9.1 TI - 20.0 9.1 10.7 3.3 - SCI 8.3 40.0 9.1 10.7 - - AI - - - - 6.7 - EI - 20.0 - 2.7 30.0 18.2 NI - - - 3.3 3.3 18.2 GO 16.7 20.0 - 2.0 3.3 - UO - - - 3.3 - - SCO 8.3 - 18.2 9.3 - - EO - - - 10.0 23.3 9.1 AO - - - - - - PI - - - - - - DISCUSSION reserve, especially during the turn of the century. The buffer zone that existed 23 years ago in the west portion Over the 23 years of bird monitoring, PEMG presented of the reserve is completely absent nowadays (L. Anjos, low species turnover and a high number of bird species pers. obs.). Other local threats have been detected over persisting over this time period. Local extinction of bird the 23 years of monitoring, like illegal hunting activities species, as well as colonization of novel bird species, and the presence of domestic species (e.g. cats and dogs) did occur in PEMG during this time period, but at in the study area (IAP 2002), threats that are known to low numbers. We argue that some features of PEMG have important impacts on biodiversity and community contributed to its relative stability, these being high dynamics (Wright 2005, Galetti & Sazima 2006, Campos number of bird species, large core area, and functional et al. 2007). The synergic effects of these threats could connectivity with other forest fragments (Laurance 2002, affect bird composition in the PEMG in terms of both Haddad et al. 2015), especially in the eastern area of local extinctions and colonizations (Laurance 2010). PEMG, which borders a large forest fragment (Lopes et al. 2006). The high number of species in P EMG, in Extinctions turn, could be explained by the natural heterogeneity of the pristine vegetation encountered in PEMG. Extinctions in the PEMG were biased towards specific This natural heterogeneity is probably the result of bird groups. This was expected because some biological topographic variation (plateau vs. hillside), which allows features are known to be better predictors of bird sensitivity for the coexistence of species with different ecological to fragmented landscapes (e.g. Henle et al. 2004, Anjos requirements in this reserve (Anjos et al. 2007, Santana 2006). For example, body size and feeding habits (Pizo & Anjos 2010). 2001, Ribon et al. 2003), dispersal capacity (Sekercioglu However, PEMG is surrounded by a human et al. 2002, Lees & Peres 2009) and geographical dominated landscape that has changed dramatically distribution (Kattan et al. 1994, Anjos et al. 2010). In our during the last 23 years. Agriculture (mainly soya beans) study, large frugivores had the highest rate of extinction has expanded over the years at the northern and western (33.3% of total extinctions) and higher number of species borders of PEMG, compromising the buffer zone of the expected to decline in the future. Ground omnivores and Revista Brasileira de Ornitologia, 24(3), 2016 Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. ground insectivores followed in terms of the number of PEMG, for example, lies over the Tropic of species that went locally extinct or presented a tendency Capricorn, a transitional region between Tropical and of future decline. These three guilds frequently show Subtropical regions and lies at the northern limit for several high sensitivity to habitat fragmentation (Thiollay 1992, bird species with a more southern distribution in Brazil. Ribon et al. 2003, Franz et al. 2010, Loures-Ribeiro et Likewise, it is at the southern limit for the distribution of al. 2011, Stratford & Stouffer 2015) due to certain several bird species with a more northern distribution in biological features that increase their susceptibility to Brazil. This peculiarity could explain some of the patterns local extinction. Large frugivores, for example, present of extinctions and declines. Species at the border of their low population densities and recruitment, and need distribution have higher probability of going extinct large living areas to feed on specific resource (Pizo 2001). because of the limited rescue effect (Anjos et al. 2010) Ground insectivores, in turn, appear to be sensitive and/or because species may be at their ecological and to microhabitat changes (e.g. in leaf litter depth and physiological limits (Kattan et al. 1994). PEMG is at the vegetation structure), which frequently occur in disturbed distributional range limit of nine bird species considered and fragmented habitats (Stratford & Stouffer 2013, as either locally extinct or possibly extinct, and seven 2015). Further, large frugivores and ground omnivores bird species considered to be declining. It is noticeable are frequently hunted due to their large body size (Strahl that species with a more southern distribution were & Grajal 1991, Pizo 2001), and terrestrial birds are more more affected (12 species, e.g. Heliobletus contaminatus, susceptible to predation by domestic species (e.g. dogs Lipaugus lanioides and Polioptila lactea) than species with and cats). a more northern distribution (4 species, e.g. Campephilus Other guilds that declined and had a high number melanoleucus and Crypturellus undulatus). of species that went “possibly extinct” were sub-canopy A possible factor responsible for the extinction bias and canopy insectivores and sub-canopy and canopy towards bird species with a more southern distributional omnivores, which are guilds that are usually not cited range is the drastic deforestation that occurred in Paraná as being prone to local extinction due to fragmentation state between 1890 and 1990 (Gubert-Filho 2010). (Bregman et al. 2014). Anjos (2006) studied the Deforestation in Paraná was severe for both semi- sensitivity of bird species in the fragmented landscape deciduous forests (that prevails in northern Paraná) of PEMG, and found that some particular species in the and araucaria forests (that occurs more to the south), aforementioned guilds (e.g. Piprites chloris and Oxyruncus eliminating the connectivity that once existed between cristatus) presented high local sensitivity to the effects of this two forest formations. Enclaves of Araucaria Forest fragmentation. However, understory insectivorous - a that were close to PEMG did occur in the past (Torezan guild that usually declines after forest fragmentation and 2002), but these have been eliminated or have become forest isolation (Stouffer & Bierregaar d 1995, Sekercioglu isolated from the core Araucaria Forest present in the south et al. 2002, Powell et al. 2015) - persisted in stable of Brazil. Thus, bir d species highly associated to Araucaria numbers in PEMG. A possible explanation could be Forest that occur in PEMG could be disappearing or the fact that we considered terrestrial species as “ground declining due to the lack of suitable habitats and absence insectivores” instead of grouping them as “understory of landscape connectivity that could allow a rescue effect. insectivores”. We think it is important to consider where This could be the case for species like H. contaminatus, in the understory these insectivore bird species forage, Piculus aurulentus and Strix hylophila. because microhabitats in the understory should differ in Climate change could also be a contributing factor their response towards fragmentation. to the decline of bird species with a more southern The extinction pattern found for P EMG follows distributional range. Changes in temperature and a widespread global pattern in tropical fragmented precipitation levels can have direct and indirect effects on landscapes, with higher extinction risk and/or declines bird populations (Crick 2004). Direct effects consist, for in insectivores and large frugivores (reviewed in Bregman example, in shifts in the reproduction period of several bird et al. 2014). However, other guilds like sub-canopy and species (Crick 2004), while indirect effects are changes in canopy omnivores were susceptible to local extinction bird resources like plants and insects (Bale et al. 2002), or decline in PEMG, a pattern of species loss that does particularly those with restricted climatic ranges or adapted not conform to the usual widespread pattern of global to lower temperatures (Butterfield & Coulson 1997). species loss in tropical fragmented landscapes (Bregman Therefore, birds as well as plants and insects associated et al. 2014). Extinctions or decline in other guilds that to colder habitats (as Araucaria Forest) could have are usually not affected by fragmentation could be related declined in PEMG due to the elevation of temperatures to particularities of the area in question, such as history, in this region (Walther et al. 2002). For example, H. time of isolation, connectivity with other forest areas and contaminatus has a specialized bill (Whitney & Pacheco surrounding matrix (Sigel et al. 2010). 1994) and a foraging strategy that involves searching Revista Brasileira de Ornitologia, 24(3), 2016 Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. arthropods in substrates (e.g. moss and lichen) that are Data limitations more common in colder regions (Parrini et al. 2009). There is little information on the avifauna of northern Colonizations Paraná state before the colonization and expansion of human activities. For instance, naturalists did not visit the th Birds species with a more northern distributional range region close to the municipality of Londrina in the 19 made up the majority of the 11 colonizing species. century. However, Peter W. Wetscot in the 1930s made For example, N. ocellatus, Amazilia lactea, Myiarchus an important account about the capture of a single Harpy tyrannulus, M. flaveo la, and Thlypopsis sor dida. Some Eagle (Harpia harpyja) individual near the municipality of these species are clearly associated with open areas, of Londrina (Scherer-Neto & Straube 1995). This like Cerrado (e.g. M. tyrannulus and M. flaveo la) (Sick record suggests that the avifauna in northern Paraná was 1997). The elevation of temperature in the region in the originally much richer in species number. Some groups, last decades (Walther et al. 2002), together with forest like great raptors (Accipitridae, e.g. Spizaetus ornatus), fragmentation that generates more open habitats for were never recorded in PEMG or the region, and their species typical of Cerrado, could explain why bird species presence can only be inferred by the use of distributional with a more northern distributional range and of drier maps. This indicates that the avifauna present in P EMG, habitats are expanding into this more moist region. An as well as the number of species locally extinct, could in emblematic case is M. flaveo la, considered a threatened fact be underestimated because of the lack of information species in Paraná, which used to have only a few records in on species distributions prior to the creation of the reserve the north of the state (Mikich & Bérnils 2004) but seems (Lees & Pimm 2015). to be currently expanding to novel areas (see WikiAves. The “indeterminate” species (species with few and com.br for current records in Paraná state). infrequent records), which were recorded only in the first The guilds with t he highest number of species years of monitoring could in fact have been common in to have colonized PEMG were edge insectivores, edge the past, but our time frame captured the presence of omnivorous, nectarivores and nocturnal insectivores. Bird these species when they were at the end of their decline. species from these guilds are mainly associated with more For example, records of Sclerurus scansor and the “Near open areas. PEMG is inserted in a fragmented landscape threatened” Phylloscartes sylviolus and P. paulista could where edge effect is favored, which could explain why have been the last ones in PEMG. The maintenance of guilds associated with open habitats were the ones with bird monitoring in PEMG can provide more information the highest number of colonizing species (Thiollay 1992, to assess the local status of such species in the future. Franz et al. 2010). To reinforce this point, as mentioned Future bird monitoring in PEMG should adopt a above, in the beginning of 2000 there was a deforestation standardized method so that different time periods can of the buffer zone, which probably increased e dge effect be appropriately compared. For example, if point counts in one of the most preserved areas of the reserve. in PEMG had a standardized protocol (e.g. the same Two carnivore species, Buteo brachyurus and Leptodon location, sampling time and radius of detection), we cayanensis, were considered as colonizers according to our would have been able to use multivariate methods such criteria. These species can be easily detected in the field as NMDS to compare bird abundance and composition because they constantly vocalize (mainly in the breeding along different time periods. We argue that it is important season) and are commonly found on thermals with to sample the same points and use the same sampling vultures (Ferguson-Lees & Christie 2001, G. Willrich, procedures used in 2014. The reason is the number of pers. obs.). This fact indicates that their absence before trails used and because points are distributed both in 2005 is not a consequence of under-sampling, but could the plateau and in the altitudinal gradient of the reserve. be a possible turnover of predators in PEMG. Forest We also advocate for the increase in the use of mist net fragmentation can lead to changes in the composition and ringing, as initiated in 2015, so that population sizes of raptors without an actual change in the number of could be estimated for several species over the years. The raptor species (Jullien & Thiollay 1996). Thus, habitat evaluation of the data obtained by these methodologies loss (promoted by agriculture expansion in the region) will allow a better comprehension of species declining together with hunting activities, both of which are tendencies in the future. considered to be the main threats to populations of large raptors (Thiollay 1985, Bildstein et al. 1998, ICMBio Implications for protected areas 2008), could have gradually eliminated large raptors from the landscape, favouring smaller raptors species that can The dynamism encountered for this bird community over tolerate more fragmented habitats, such as the species the years was weak, which indicates that most bird species mentioned above. were able to persist/occupy PEMG after it was declared a Revista Brasileira de Ornitologia, 24(3), 2016 Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. P. & Carvalho, J. 2011. Bird species abundance-occupancy legal reserve. If we consider the avifauna list of Scherer- patterns and sensitivity to forest fragmentation: implications Neto et al. (2011), PEMG harbors almost 45% of all for conservation in the Brazilian Atlantic Forest. Biological bird species present in Paraná state, and together with the Conservation, 144: 2213–2222. small species dynamism over the years, the role of PEMG Anjos, L.; Collins, C. D.; Holt, R. D.; Volpato, G. H.; Lopes, E. for the conservation of biodiversity in northern Paraná V.; Bochio, G. M. 2015. Can habitat specialization patterns of Neotropical birds highlight vulnerable areas for conservation in is undeniable. Like many other protected areas, PEMG the Atlantic Rainforest, southern Brazil? Biological Conservation, is under constant pressure. For example, a recent plan to 188: 32–40. build an airport in the vicinity of PEMG was rejected due Anjos, L. & Ferreira, A. R. J. 1998. Registros de campo de Hylocharis to the efforts of the Instituto Ambiental do Paraná (IAP) sapphirina e H. cyanus na região de Londrina, norte do Estado do Paraná, sul do Brasil (Trochiliformes: Trochilidae).  Revista and a local NGO (MAE). However, other development Brasileira de Ornitologia, 6: 51. projects such as the implementation of industries next to Anjos, L.; Holt, R. D. & Robinson, S. 2010. Position in the PEMG are still under discussion. distributional range and sensitivity to forest fragmentation Furthermore, in a new concept of conservation called in birds: a case history from the Atlantic Forest, Brazil. Bird Conservation International, 20: 392–399. “biodiversity-friendly landscapes”, which aims to create a Anjos, L. & Schuchmann, K. L. 1997. Biogeographical affinities of more functional and connected landscape that conciliates the avifauna of the Tibagi River Basin, Parana drainage system, human necessities and biodiversity conservation (Melo et southern Brazil. Ecotropica, 3: 43–65. al. 2013), PEMG could act as a source for many bird Anjos, L.; Schuchmann, K. L. & Berndt, R. 1997. Avifaunal populations that could expand to surrounding areas composition, species richness and status in the Tibagi River Basin, Parana state, southern Brazil. Ornitología Neotropical, 8: 145–173. of less preserved forest fragments or new restoration Anjos, L.; Volpato, G. H.; Lopes, E. V.; Serafini, P. P.; Poletto, F . areas (Brancalion et al. 2013). Together with the use of & Aleixo, A. 2007. The importance of riparian forest for the ecological corridors and restoration areas that increase maintenance of bird species richness in an Atlantic Forest remnant, connectivity within this highly fragmented landscape, it is southern Brazil. Revista Brasileira de Zoologia, 24: 1078–1086. possible to increase rescue effects among bird populations Anjos, L.; Zanette, L. & Lopes, E. V. 2004. Effects of fragmentation on the bird guilds of the Atlantic Forest in north Paraná, southern of nearby forest fragments, thus increasing the chances of Brazil. Ornitología Neotropical, 15: 137–144. maintaining current biodiversity in the long run. Bale, J.; Masters, G. J.; Hodkinson, I. D.; Awmack, C.; Bezemer, T. M.; Brown, V. K.; Butterfield, J.; Buse, A.; Coulson, J. C.; Farrar, J.; Good, J. E. G.; Harrington, R.; Hartley, S.; Jones, T. H.; Lindroth, R. L.; Press, M. C.; Symrnioudis, I.; Watt, A. ACKNOWLEDGEMENTS D. & Whittaker, J. B. 2002. Herbivory in global climate change research: direct effects of rising temperature on insects herbivores. CAPES provided scholarships to G. Willrich, L. C. Global Change Biology, 8: 1–16. Calsavara, G. M. Bochio and G. L. M. Rosa. L. dos Anjos Bencke, G. A.; Mauricio, G. N.; Develey, P. F. & Goerk, J. M. (eds.). received a grant form CNPq (306293/2014-5) during 2006. Áreas importantes para a conservação das aves no Brasil: Parte 1 - Estados do domínio da Mata Atlântica. São Paulo: SAVE Brasil. the development of this study. IAP, ICMBio and IBAMA Bernarde, P. S. & Anjos, L. 1999. Distribuição espacial e temporal provided research licenses (IAP No. 33.14 and No. 40.14; da anurofauna no Parque Estadual da Mata dos Godoy, Londrina, SISBIO No. 45092-1; IBAMA/CEMAVE No. 3892/1) Paraná, Brasil (Amphibia: Anura). Comunicação do Museu de for bird monitoring and logistic support was provided by Ciências e Tecnologia da PUCRS, Série Zoologia, 12: 127–140. Bernarde, P. S & Machado, R. A. 2006. Répteis Squamata do Parque PEMG employees. We would also like to thank Edson Estadual Mata dos Godoy, p. 114–120. In: Torezan, J. M. D. (ed.). Mendes Francisco and Rafael Campos de Barros for Ecologia do Parque Estadual Mata dos Godoy. Londrina: Itedes. helping during fieldwork in 2014. We also thank the Bibby, C. J.; Burgess, N. D. & Hill, D. A. 1993. 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Nomenclature of species follows Piacentini et al. (2015) and endemic species (E) of Atlantic Forest follows Bencke et al. (2006). Literature review and unpublished data before 2005 (in parenthesis the period of sampling): 1) Anjos et al. 1997 (1993–1996); 2) Anjos & Ferreira 1998 (1997); 3) Anjos 2001 (1996); 4) Anjos et al. 2004 (1997); 5) Anjos field works (1993, 1995–1999); 6) Anjos field works (2001–2002); 7) Anjos et al. 2007 (2001); 8) Lopes et al. 2006 (2003–2004); 9) Anjos et al. 2011 and unpublished data (2004–2005). Literature review and unpublished data after 2005 (in parenthesis the period of sampling): 10) Santana & Anjos 2010 (2007); 11) Bochio & Anjos 2012 (2009–2010); 12) Bochio field works (2009–2010); 13) O liveira field works (2009–2015); 14) Muzi field works (2010–2012); 15) Zaiden et al. 2015 (2011); 16) Rosa field works (2009– 2015); 17) Calsavara field works (2013–2015); Willrich field works (2014–2015); Mist nets (2015). Local Status: FP – forest persistent; NFP – non-forest persistent; D – forest persistent and declining; PE – possibly extinct; EX – extinct; FM – frequent migrant; OF – occasional migrant; C – colonizer; S – sporadic species; I – indeterminate. Conservation Status: VU – vulnerable; EN – endangered; CR – critically endangered; NT – near threatened; DD – data deficient; PR – regional level (Mikich & Bérnils 2004); BR – national level (ICMBio 2014); GL – global level (IUCN 2015). Guilds: CA – carnivores; CE – carrion eaters; LF – large frugivores; SF – small frugivores; SE – seedeaters; NE – nectarivores; GI – ground insectivores; UI – understory insectivores; TI – trunk and twig insectivores; SCI – sub-canopy and canopy insectivores; AI – aerial insectivores; EI – edge insectivores; NI – nocturnal insectivores; GO – ground omnivores; UO – understory omnivores; SCO – sub-canopy and canopy omnivores; EO – edge omnivores; AO – aquatic omnivores and PI – piscivorous. Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Tinamidade                              Tinamus solitarius (Vieillot, 1819) E X   XXXXX   X             PE NT-GL; VU-PR GO Crypturellus obsoletus (Temminck, 1815) X   XXXXX   X   XXXX   X   X   FP   GO Crypturellus undulatus (Temminck, 1815) X   X   X                   EX CR-PR GO Crypturellus parvirostris (Wagler, 1827) X  X  X  X  X   X X X    X  X  FP   GO Crypturellus tataupa (Temminck, 1815) X   XXX   X   X   XXXX   XXX   FP   GO Rhynchotus rufescens (Temminck, 1815)                 X    X   X   S   GO Nothura maculosa (Temminck, 1815) X                X X     X   NFP   GO Anatidae                              Dendrocygna viduata (Linnaeus, 1766) X                       S   AO Cracidae                              Penelope superciliaris Temminck, 1815 X   XXXXX   X   XXXXXXXX   FP   LF Aburria jacutinga (Spix, 1825) E X   X                     EX EN-GL; EN-BR; EN-PR LF Crax fasciolata Spix, 1825 X   X                     EX VU-GL; CR-PR LF Odontophoridae                              Odontophorus capueira (Spix, 1825) E X                       EX   GO Ardeidae                              Nycticorax nycticorax (Linnaeus, 1758)                 X      X   S   AO Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Butorides striata (Linnaeus, 1758)                 X        S   AO Bubulcus ibis (Linnaeus, 1758 X                     X   S   GO Ardea cocoi Linnaeus, 1766                    X     S   AO Ardea alba Linnaeus, 1758                    X     S   AO Syrigma sibilatrix (Temminck, 1824)                      X   S   GO Egretta thula (Molina, 1782)                    X     S   AO Threskiornithidae                              Mesembrinibis cayennensis (Gmelin, 1789)                      X   S NT-PR AO Theristicus caudatus (Boddaert, 1783)                 X        S   GO Cathartidae                              Cathartes aura (Linnaeus, 1758) X                X    X   X   FP   CE Coragyps atratus (Bechstein, 1793) X                X    X X X   FP   CE Sarcoramphus papa (Linnaeus, 1758) X                   X X X   FP   CE Accipitridae                              Leptodon cayanensis (Latham, 1790)                 X      X   C   CA Elanoides forficatus (Linnaeus, 1758) X                X    X   X   FM   AI Elanus leucurus (Vieillot, 1818) X                X    X     NFP   CA Harpagus diodon (Temminck, 1823) X                       OM   CA Accipiter striatus Vieillot, 1808 X       X          X        FP   CA Ictinia plumbea (Gmelin, 1788) X     X X X   X      X    X   X   FM   AI Heterospizias meridionalis (Latham, 1790)                      X   S   CA Rupornis magnirostris (Gmelin, 1788) X       X   X      X    X X X   FP   CA Geranoaetus albicaudatus (Vieillot, 1816)                 X        S   CA Buteo nitidus (Latham, 1790) X                       I   CA Buteo brachyurus Vieillot, 1816                 X X     X   C   CA Aramidae                               Aramus guarauna (Linnaeus, 1766)                       X   S   AO Rallidae                              Aramides saracura (Spix, 1825) E X     X   X   X   X X X      X   FP   GI Laterallus melanophaius (Vieillot, 1819) X                       I   GI Pardirallus nigricans (Vieillot, 1819)                      X   I   GI Charadriidae                              Vanellus chilensis (Molina, 1782) X                X    X   X   NFP   GI Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Columbidae                              Columbina talpacoti (Temminck, 1810) X                X    X X X   FP   SE Columbina squammata (Lesson, 1831) X                X    X     FP   SE Columbina picui (Temminck, 1813) X                X    X   X   NFP   SE Claravis pretiosa (Ferrari-Perez, 1886) X       X   X   X X    X    X   FP   LF Patagioenas picazuro (Temminck, 1813) X   XXXXX   X   XXX   XXXX   FP   EO Patagioenas cayennensis (Bonnaterre, 1792) X   XXXXX   X   XXX   XX   X   FP   LF Patagioenas plumbea (Vieillot, 1818) X   X                X      D   LF Zenaida auriculata (Des Murs, 1847) X                X    X X X   NFP   EO Leptotila verreauxi Bonaparte, 1855 X   XXXXX   X   XXXXXXXX   FP   LF Leptotila rufaxilla (Richard & Bernard, 1792) X   XXX   X   X   XXXXXX   X   FP   LF Geotrygon montana (Linnaeus, 1758) X   XXXXX   X   XXXXXX   X   FP   LF Cuculidae                              Piaya cayana (Linnaeus, 1766) X   XXXXX   X   XXXX   XXX   FP   SCI Coccyzus melacoryphus Vieillot, 1817 X    X      X   X X X      X   FM   EI Coccyzus americanus (Linnaeus, 1758) X    X   X X   X             OM   SCO Coccyzus euleri Cabanis, 1873 X      X X                 OM DD-PR SCI Crotophaga ani Linnaeus, 1758 X   X              X    X   X   NFP   EI Guira guira (Gmelin, 1788) X                X    X X X   NFP   EI Tapera naevia (Linnaeus, 1766) X       XX         XX   X   XXX   FP   EI Dromococcyx pavoninus Pelzeln, 1870 X         X   XXXX   X   X   FP   UI Tytonidae                              Tyto furcata (Temminck, 1827) X                X    X   X   FP   CA Strigidae                              Megascops choliba (Vieillot, 1817) X       X          X X   X   X   FP   NI Pulsatrix perspicillata (Latham, 1790) X   X   X                   EX VU-BR; DD-PR CA Pulsatrix koeniswaldiana (Bertoni & Bertoni, 1901) E X   XXXX             X     X   X   FP   CA Bubo virginanus (Gmelin, 1788) X                       S   CA Strix hylophila Temminck, 1825 E X   X   X               X     D NT-GL CA Strix virgata (Cassin, 1849)                      X   I DD-PR CA Glacidium brasilianum (Gmelin, 1788) X  X X X  X  X       X    X  X  FP   NI Athene cunicularia (Molina, 1782) X                X    X   X   NFP   NI Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Th Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Nyctibiidae                              Nyctibius aethereus (Wied, 1820) X                       I EN-BR; DD-PR NI Nyctibius griseus (Gmelin, 1789) X                X    X   X   FP   NI Caprimulgidae                              Nyctiphrynus ocellatus (Tschudi, 1844)                 X    X   X   C EN-PR NI Antrostomus rufus (Boddaert, 1783) X                   X     FP   NI Lurocalis semitorquatus (Gmelin, 1789) X   X              X      X   FM   NI Nyctidromus albicollis (Gmelin, 1789) X               X X    X   X   FP   NI Hydropsalis parvula (Gould, 1837)                    X   X   C   NI Hydropsalis torquata (Gmelin, 1789)                 X        S   NI Podager nacunda (Vieillot, 1817) X                X      X   FM   NI Chordeiles minor (Forster, 1771) X                       OM DD-PR NI Chordeiles acutipennis (Hermann, 1783) X                       OM   NI Apodidae                              Cypseloides fumigatus (Streubel, 1848)                 X        S   AI Streptoprocne zonaris (Shaw, 1796) X                X        S   AI Chaetura cinereiventris Sclater, 1862 X                     X   OM   AI Chaetura meridionalis Hellmayr, 1907 X                X    X   X   FM   AI Trochilidae                              Phaethornis squalidus (Temminck, 1822) E                 X        I   NE Phaethornis pretrei (Lesson & Delattre, 1839) X                X        FP   NE Phaethornis eurynome (Lesson, 1832) E X  X  X X X  X       X X  X  X  FP   NE Eupetomena macroura (Gmelin, 1788) X                X    X X    FP   NE Florisuga fusca (Vieillot, 1817) E X                     X   FP   NE Colibri serrirostris(Vieillot, 1816) X                       I   NE Anthracothorax nigricollis (Vieillot, 1817) X   X X             X    X     FP   NE Stephanoxis lalandi (Vieillot, 1818) E X                   X     I   NE Chlorostilbon lucidus (Shaw, 1812) X    X    X   X      X X     X   FP   NE alur ania glaucopis (Gmelin, 1788) E X     XXXX   X       XX       X   FP   NE Hylocharis sapphirina (Gmelin, 1788) X                       I   NE Hylocharis cyanus (Vieillot, 1818)   X                      I   NE Hylocharis chrysura (Shaw, 1812) X                X X   X   X   FP   NE Leucochloris albicollis (Vieillot, 1818) E X                X        OM   NE Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Amazilia versicolor (Vieillot, 1818)                 X X     X   C   NE Amazilia fimbriata (Gmelin, 1788) X                   X   X   FP   NE Amazilia lactea (Lesson, 1832)                 X X   X     C   NE Trogonidae                             Trogon surrucura Vieillot, 1817 E X   XXXXX   X   XXXXXXXX   FP   SCO Trogon rufus Gmelin, 1788 X   XXXXX   X   XXXXXXXX   FP   SCO Alcedinidae                             Megaceryle torquata (Linnaeus, 1766)                      X   I   PI Chloroceryle amazona (Latham, 1790)                      X   I   PI Momotidae                              Baryphthengus ruficapillus (Vieillot, 1818) E X   XXXXX   X   XXXXXXXXX FP   UI Galbulidae                              Galbula ruficauda Cuvier, 1816 X                       I NT-PR EI Bucconidae                             Notharchus swainsoni (Gray, 1846) E X   X              X      X   FP   SCO Nystalus chacuru(Vieillot, 1816) X                       S   EO Nonnula rubecula (Spix, 1824) X     X     X       XXXX   XXXX FP   UI Ramphastidae                              Ramphastos dicolorus Linnaeus, 1766 E X   XXX   X   X   XXXXXXXX   FP   SCO Selenidera maculirostris (Lichtenstein, 1823) E X   XXXXX   X   XXXXXXXX   FP   SCO Pteroglossus bailloni (Vieillot, 1819) E X   X   X   X       XXXXX     X   FP NT-GL SCO Pteroglossus aracari (Linnaeus, 1758) X   XXXXX       X     X       D VU-PR SCO Pteroglossus castanotis Gould, 1834                    X   X   I   SCO Picidae                             Picumnus cirratus Temminck, 1825              X    X       I   TI Picumnus temminckii Lafresnaye, 1845 E X   XXXXX   X       XX   XXX   FP   TI Picumnus nebulosus Sundevall, 1866 X                       I NT-GL TI Melanerpes candidus (Otto, 1796) X                X    X X X   FP   TI Melanerpes flavifrons (Vieillot, 1818) E X   XXXXX   X   XXXX   XXX   FP   TI Veniliornis spilogaster (Wagler, 1827) E X   XXXXX   X   XXXX       X   FP   TI Piculus aurulentus (Temminck, 1821) E X    X X X           X        D NT-GL TI Colaptes melanochloros (Gmelin, 1788) X   XXXX         XXXX   X   X   NFP   TI Colaptes campestris (Vieillot, 1818) X                X    X   X   FP   TI Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Th Th Th Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Celeus flavescens (Gmelin, 1788) X   XXX           XX   X   XXX   FP   TI Dryocopus lineatus (Linnaeus, 1766) X   XXXXX   X   XXXX   X   X   FP   TI Campephiluss robustus (Lichtenstein, 1818) E X    X X          X X X    X  X  FP   TI Campephilus melanoleucos (Gmelin, 1788)     XXXX                   PE   TI Falconidae                              Caracara plancus (Miller, 1777) X       X       X X X    X   X   NFP   CA Milvago chimachima (Vieillot, 1816) X                X    X   X   NFP   CA Herpetotheres cachinnans (Linnaeus, 1758) X   XXXXX   X          X   X   FP   CA Micrastur ruficollis (Vieillot, 1817) X  X  X X X          X    X  X  FP   CA Micrastur semitorquatus (Vieillot, 1817) X   XXXXX   X   XXXX   XXX   FP   CA Falco sparverius Linnaeus, 1758 X                X    X   X   NFP   AI Falco femoralis Temminck, 1822 X                X        NFP   CA Falco peregrinus Tunstall, 1771                 X      X   OM   CA Psittacidae                             Primolius maracana (Vieillot, 1816) X     XXXX       X       X      D NT-GL; EN-PR LF Psittacara leucophthalmus (Statius Muller, 1776) X   XXXXX   X   XXXXXXXX   FP   LF Aratinga auricapillus (Kuhl, 1820) X   X   XXX   X   XXXXXXXX   FP NT-GL LF Eupsittula aurea (Gmelin, 1788) X                       S   LF Pyrrhura frontalis (Vieillot, 1817) E X   XXXXX   X   XXXXXXXX   FP   LF Forpus xanthopterygius (Spix, 1824) X  X  X              X    X  X  FP   EO Brotogeris tirica (Gmelin, 1788) E X  X  X X X  X   X X X  X X  X  FP   LF Pionopsitta pileata (Scopoli, 1769) E X   XXXXX   X   XXX   XX   X   FP   LF Pionus maximiliani (Kuhl, 1820) X   XXXXX   X   XXXXXXXX   FP   LF Amazona aestiva (Linnaeus, 1758) X   XXXXX   X   XXXXXX   X   FP   LF Triclaria malachitacea (Spix, 1824) E X   XXXXX       X       X      D NT-GL; VU-PR LF Thamnophilidae                              Dysithamnus mentalis (Temminck, 1823) X   XXXXXX X   XXXX   X   XX FP   UI Herpsilochmus rufimarginatus (Te mminck, 1822) X   XXXXXX X   XXX     X   X   FP   SCI amnophilus doliatus (Linnaeus, 1764) X      X           X    X     FP   EI amnophilus ruficapillus Vieillot, 1816 X                X    X   X   NFP   EI amnophilus caerulescens Vieillot, 1816 X   XXXXXX X   XXX     X   X   FP   UI Hypoedaleus guttatus (Vieillot, 1816) E X   XXXXXX X   XXXX   XXX   FP   SCI Mackenziaena leachii (Such, 1825) E       X X   X             I   UI Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Mackenziaena severa (Lichtenstein, 1823) E X     XXXXX X X XXXX   X   X   FP   UI Pyriglena leucoptera (Vieillot, 1818) E X   XXXXXX X X XXXX   XXXX FP   UI Drymophila rubricollis (Bertoni, 1901) E X    X    X     X    X      X   FP   UI Drymophila malura (Temminck, 1825) E X   X X X   X     X    X        FP   UI Conopophagidae                              Conopophaga lineata (Wied, 1831) E X   XXXXX   X X XXX     XXXX FP   UI Grallariidae                              Grallaria varia (Boddaert, 1783) X   X X X   X   X      X        D   GI Hylopezus nattereri (Pinto, 1937) E        X     X    X        D   GI Rhinocryptidae                              Eleoscytalopus indigoticus (Wied, 1831) E X   XXX   X       XXXX     XX   FP   UI Psilorhamphus guttatus (Ménétriès, 1835) E X   X X X   X          X      X   FP NT-PR UI Formicariidae                              Chamaeza campanisona (Lichtenstein, 1823) X   XXXXX   X   XXX      X   FP   GI Chamaeza ruficauda (Cabanis & Heine, 1859) E X                       EX   GI Scleruridae                              Sclerurus scansor (Ménétriès, 1835) E X   X                     I   GI Dendrocolaptidae                             Dendrocincla turdina (Lichtenstein, 1820) E X   XXXXX   X   XXXX   XXXX FP   TI Sittasomus griseicapillus (Vieillot, 1818) X   XXXXX   X   XXXX   XXXX FP   TI Xiphorhynchus fuscus (Vieillot, 1818) E X   XXXXX   X   XXXX   X   XX FP   TI Campylorhamphus falcularius (Vieillot, 1822) E        X       XXXX   X   X   FP   TI Lepidocolaptes angustirostris (Vieillot, 1818)       XXXX               X   S NT-PR TI Dendrocolaptes platyrostris Spix, 1825 X   XXXXX   X   XXXX   X   X   FP   TI Xiphocolaptes albicollis (Vieillot, 1818) X   XXXXX   X   XXXX   X   X   FP   TI Xenopidae                              Xenops rutilans Temminck, 1821 X   XXXXX   X   XXXX   XXX   FP   TI Furnariidae                             Furnarius rufus (Gmelin, 1788) X                X    X   X   NFP   EO Lochmias nematura (Lichtenstein, 1823)        X          X    X   X   FP   UI Clibanornis dendrocolaptoides (Pelzeln, 1859)E    X                     I NT-GL UI Automolus leucophthalmus (Wied, 1821) E X   X   X   X   X X XXXX   XXXX FP   UI Anabacerthia lichtensteini (Cabanis & Heine, 1859) E     XXXXX   X   XXXX   X   X   FP   SCI Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Philydor rufum (Vieillot, 1818) X   XXXXX   X       XX   XXX   FP   SCI Heliobletus contaminatus Pelzeln, 1859 E X   X   X X X     X           D   SCI Syndactyla rufosuperciliata (Lafresnaye, 1832) X  X  X      X       X    X  X  FP   UI Synallaxis ruficapilla Vieillot, 1819 E X   XXXXX   X X XXXX   XXXX FP   UI Synallaxis cinerascens Temminck, 1823 X   XXX   X     X XXXX   XXX   FP   UI Synallaxis frontalis Pelzeln, 1859 X   X   X           XXX     XXX   NFP   EI Synallaxis spixi Sclater, 1856 X   XXX           XXX     X   X   NFP   EI Cranioleuca obsoleta (Reichenbach, 1853) E     XXXXX   X X XXX      X   FP   TI Pipridae                              Pipra fasciicauda Hellmayr, 1906 X   X   X   X       XXXX       FP   SF Manacus manacus (Linnaeus, 1766) X   X   X                   EX   SF Chiroxiphia caudata (Shaw & Nodder, 1793) E X   XXXXX   X   XXXX   XXXX FP   SF Oxyruncidae                              Oxyruncus cristatus Swainson, 1821 X   X X X         X X         D   SCO Onychorhynchidae                             Myiobius barbatus (Gmelin, 1789) X                       I   UI Tityridae                              Schiffornis virescens (Lafresnaye, 1838) E X     X         X X X    X     FP   UO Tityra inquisitor (Lichtenstein, 1823) X   X   X   X   X   XXXX   X       FP   LF Tityra cayana (Linnaeus, 1766) X   XXXXX   X   XXXX   X   X   FP   LF Pachyramphus viridis (Vieillot, 1816) X   X              X    X     FM   SCI Pachyramphus castaneus (Jardine & Selby, 1827) X   XXXXX   X       X     X   X   FP   SCI Pachyramphus polychopterus (Vieillot, 1818) X      X X       XXXX   X   X   FM   SCI Pachyramphus validus (Lichtenstein, 1823) X  X  X X X          X X  X  X  FM   SCI Contigidae                             Phibalura flavirostris Vieillot, 1816 X                       I NT-GL; NT-PR SCO Pyroderus scutatus (Shaw, 1792) E                  X       I NT-PR LF Lipaugus lanioides (Lesson, 1844) E X                       EX NT-GL; NT-PR LF Procnias nudicollis (Vieillot, 1817) E      X                   EX VU-GL LF Pipritidae                              Piprites chloris (Temminck, 1822) X   X X X   X                 PE   SCI Platyrinchidae                              Platyrinchus mystaceus Vieillot, 1818 X     XX   X   X X XXXX   XXXX FP   UI Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Rhynchocyclidae                              Mionectes rufiventris Cabanis, 1846 E X   XXXXX           X        FP   UO Leptopogon amaurocephalus Tschudi, 1846 X   XXXXX   X   XXXX   XXX   FP   UI Corythopis delalandi (Lesson, 1830) X       X   X X XXXX   XXXX FP   UI Phylloscartes eximius (Temminck, 1822) E X   X   X                   EX NT-GL SCI Phylloscartes ventralis (Temminck, 1824) X   XXXXX       XX       XX     FP   SCI Phylloscartes paulista Ihering & Ihering, 1907 E X I NT-GL; NT-PR SCI Phylloscartes sylviolus (Cabanis & Heine, 1859) E X                       I NT-GL; DD-PR SCI Tolmomyias sulphurescens (Spix, 1825) X   XXXXX   X   XXXX   XXX   FP   SCI Todirostrum cinereum (Linnaeus, 1766) X       X          X    X   X   FP   EI Poecilotriccus plumbeiceps (Lafresnaye, 1846) X   XXXXX     X     X     X   X   FP   UI Myiornis auricularis (Vieillot, 1818) E X   XXXXX   X X     X     XXX   FP   SCI Hemitriccus diops (Temminck, 1822) E        X     X    X    X   X   FP   UI Hemitriccus obsoletus (Miranda-Ribeiro, 1906) E X       X       X X X        FP DD-PR UI Hemitriccus margaritaceiventer (d'Orbigny & Lafresnaye, 1837) X                   X     S   EI Tyrannidae                              Hirundinea ferruginea (Gmelin, 1788)                 X        S   EI Euscarthmus meloryphus Wied, 1831 X                     X   S   EI Tyranniscus burmeisteri (Cabanis & Heine, 1859) X     X     X   X X       X   FP DD-PR SCI Camptostoma obsoletum (Temminck, 1824) X   XXXXX   X   XXX     X   X   FP   SCO Elaenia flavo gaster (Thunberg, 1822) X                X      X   FP   EO Elaenia parvirostris Pelzeln, 1868 X                X X   X   X   FM   EO Elaenia mesoleuca (Deppe, 1830) X   X     X             X     FM   EO Elaenia chiriquensis Lawrence, 1865                      X   OM   EO Elaenia obscura (d'Orbigny & Lafresnaye, 1837)                      X   I   EO Myiopagis caniceps (Swainson, 1835) X   XXXXX   X   XXXX   X   X   FP   SCI Myiopagis viridicata (Vieillot, 1817) X   X              X    X   X   FP   SCI Capsiempis flaveo la (Lichtenstein, 1823) X  X X X  X    X     X    X  X  FP   UI Phyllomyias virescens (Temminck, 1824) E                      X   I   SCI Serpophaga subcristata (Vieillot, 1817) X                X    X   X   NFP   EI Legatus leucophaius (Vieillot, 1818)              XXXX   X   X   FM   SCI Myiarchus swainsoni Cabanis & Heine, 1859 X       XXX   X     XX     X   X   FM   SCI Myiarchus ferox (Gmelin, 1789)                 X    X   X   C   EI Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Myiarchus tyrannulus (Statius Muller, 1776)                 X    X   X   C   EI Sirystes sibilator (Vieillot, 1818) X   XXXXX   X   XXXX   XXX   FP   SCI Pitangus sulphuratus (Linnaeus, 1766) X  X  X  X  X   X X X    X  X  FP   EO Machetornis rixosa (Vieillot, 1819) X                X    X   X   NFP   EI Myiodynastes maculatus (Statius Muller, 1776) X   XXXXX   X   XXXX   XXX   FM   EO Megarynchus pitangua (Linnaeus, 1766) X   XXXXX   X   XXXX   XXX   FP   EO Myiozetetes similis (Spix, 1825) X  X X X  X          X    X  X  FP   EO Tyrannus melancholicus Vieillot, 1819 X  X  X              X    X  X  FM   EI Tyrannus savana Daudin, 1802 X                X    X   X   FM   EO Empidonomus varius (Vieillot, 1818) X       X          X    X   X   FM   EO Colonia colonus (Vieillot, 1818) X   XXXX     X       X     X   X   FP   SCI Myiophobus fasciatus (Statius Muller, 1776) X   X X             X X   X   X   FM   EI Pyrocephalus rubinus (Boddaert, 1783) X                X    X     FM   EI Arundinicola leucocephala (Linnaeus, 1764) X                       S   EI Cnemotriccus fuscatus (Wied, 1831) X           X X X X    X   X   FM   EI Lathrotriccus euleri (Cabanis, 1868) X   X   XXX   X X XXXX   X   XX FM   UI Contopus cinereus (Spix, 1825) X                X      X   FP   SCI Knipolegus cyanirostris (Vieillot, 1818) X                     X   FP   EI Satrapa icterophrys (Vieillot, 1818) X                       S   EI Muscipipra vetula (Lichtenstein, 1823) E X                       S   SCI Vireonidae                             Cyclarhis gujanensis (Gmelin, 1789) X   XXXXX   X   XXX     XXX   FP   SCO Hylophilus poicilotis Temminck, 1822 E X       X                 PE   EI Vireo chivi (Vieillot, 1817) X       X   X      X    X   X   FM   SCO Corvidae                              Cyanocorax chrysops (Vieillot, 1818) X   XXXXX   X   XXXX   XXX   FP   EO Hirundinidae                              Pygochelidon cyanoleuca (Vieillot, 1817) X                X X   X   X   NFP   AI Alopochelidon fucata (Temminck, 1822) X                       OM   AI Stelgidopteryx ruficollis (Vieillot, 1817) X                X X   X   X   FM   AI Progne tapera (Vieillot, 1817) X                X    X   X   FM   AI Progne chalybea (Gmelin, 1789) X                X      X   FM   AI Tachycineta leucorrhoa (Vieillot, 1817) X                     X   FM   AI Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Hirundo rustica Linnaeus, 1758 X                       OM   AI Petrochelidon pyrrhonota (Vieillot, 1817) X                       OM   AI Troglodytidae                              Troglodytes musculus Naumann, 1823 X   X       X       XXX     XXX   NFP   EI Polioptilidae                              Polioptila lactea Sharpe, 1885 E X   X X X   X                 PE NT-GL; EN-PR SCI Turdidae                              Turdus leucomelas Vieillot, 1818 X   XXXXX   X   XXXX   XXXX FP   EO Turdus rufiventris Vieillot, 1818 X   X   XXX   X   XXX     XXXX FP   EO Turdus amaurochalinus Cabanis, 1850 X  X X  X X  X   X X X    X  X  FP   EO Turdus subalaris (Seebohm, 1887) E       X X         X X X   X X X   FM   UO Turdus albicollis Vieillot, 1818 X   X   X   X   X   XXXX     XXX FP   UO Mimidae                              Mimus saturninus (Lichtenstein, 1823) X                X    X   X   NFP   EO Motacillidae                              Anthus lutescens Pucheran, 1855 X                X    X   X   NFP   EO Passerellidae                              Zonotrichia capensis (Statius Muller, 1776) X       X          X    X   X   NFP   SE Ammodramus humeralis (Bosc, 1792) X                X    X   X   NFP   EO Arremon semitorquatus Swainson, 1838 E                 X        I   SE Arremon flavirostris Swainson, 1838                 X        S   SE Parulidae                              Setophaga pitiayumi (Vieillot, 1817) X   XXXXX       XXXX   XXX   FP   SCI Geothlypis aequinoctialis (Gmelin, 1789) X                X    X   X   NFP   EI Basileuterus culicivorus (Deppe, 1830) X   XXXXX   X   XXX     XXXX FP   UI Myiothlypis flaveo la Baird, 1865          X      X X   X X X   C VU-PR EI Myiothlypis leucoblephara (Vieillot, 1817) E X   XXX   X       XXX     XXXX FP   UI Icteridae                             Cacicus chrysopterus (Vigors, 1825)                 X        I   SCO Cacicus haemorrhous (Linnaeus, 1766) X   XXXXX   X   XXXX   XXX   FP   SCO Icterus pyrrhopterus (Vieillot, 1819) X                X        FP   EO Gnorimopsar chopi (Vieillot, 1819) X                       S   EO Molothrus oryzivorus (Gmelin, 1788) X                       S   EO Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Th Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Molothrus bonariensis (Gmelin, 1789) X                X    X   X   NFP   EO Sturnella superciliaris (Bonaparte, 1850) X                X    X     NFP   EO Thraupidae                              Pipraeidea melanonota (Vieillot, 1819) X     XXXX   X       XX   X   X   FP   SCO Cissopis leverianus (Gmelin, 1788) X   XXXXX           X     X   X   FP   LF Tangara seledon (Statius Muller, 1776) E X                       I   SCO Tangara sayaca (Linnaeus, 1766) X   XXXXX   X   XXX     X   X   FP   EO Tangara preciosa (Cabanis, 1850) X                X X       FP   EO Tangara cayana (Linnaeus, 1766) X                       I NT-PR EO Nemosia pileata (Boddaert, 1783) X                X    X   X    FP   SCO Conirostrum speciosum (Temminck, 1824) X   XXXXX   X   XXXX   X   X   FP   SCO Sicalis flaveo la (Linnaeus, 1766)                    X   X   S   SE Haplospiza unicolor Cabanis, 1851 E                 X      X   C   SE Hemithraupis guira (Linnaeus, 1766) X   XXXXX   X   XXXX   X   X   FP   SCO Volatinia jacarina (Linnaeus, 1766) X                X X   X   X   FM   SE Trichothraupis melanops (Vieillot, 1818) X   XXXXX   X   XXXX   XXXX FP   UO Coryphospingus cucullatus (Statius Muller, 1776) X                X X   X   X   NFP   SE Tachyphonus coronatus (Vieillot, 1822) E X   XXXXX       XXX     X   X   FP   EO Ramphocelus carbo (Pallas, 1764) X                       S   EO Tersina viridis (Illiger, 1811) X       X   X      X X   X   X   FM   SF Dacnis cayana (Linnaeus, 1766) X       X   X   XXXX   X   X   FP   SCO Coereba flaveo la (Linnaeus, 1758) X                X    X   X   FP   NE Tiaris fuliginosus (Wied, 1830) X                       EX   SE Sporophila lineola (Linnaeus, 1758)                 X        S   SE Sporophila collaris (Boddaert, 1783) X                       S   SE Sporophila caerulescens (Vieillot, 1823) X                   X   X   NFP   SE Saltator similis d'Orbigny & Lafresnaye, 1837 X   X   XXX   X   XXXX   X   XX FP   EO Saltator fuliginosus (Daudin, 1800) E X   XXXXX   X   XXX       XX   FP   LF lypopsis sor dida (d'Orbigny & Lafresnaye, 1837)                 X    X     C   EO Pyrrhocoma ruficeps (Strickland, 1844) E X      X  X          X X  X  X  FP   UI Cardinalidae                              Piranga flav a (Vieillot, 1822) X                       EX NT-PR SCO Habia rubica (Vieillot, 1819) X   XXXXX   X     XX     XXX   FP   UO Twenty-three years of bird monitoring reveal low extinction and colonization of species in a reserve surrounded by an extremely fragmented landscape in southern Brazil Guilherme Willrich et al. Revista Brasileira de Ornitologia, 24(3), 2016 Before 2005 After 2005 Local Family/species Conservation Status Guild Status 1 2 3 4 5 6 7 8 9 10 111213141516171819 Amaurospiza moesta (Hartlaub, 1853) E                 X        I NT-GL SE Cyanoloxia brissonii (Lichtenstein, 1823) X                       I   SE Fringillidae                              Spinus magellanicus (Vieillot, 1805) X                       S   SE Euphonia chlorotica (Linnaeus, 1766) X   XXXXX   X   XXX     XXX   FP   SF Euphonia violacea (Linnaeus, 1758) X   XXX           XXX     X   X   FP   SF Euphonia cyanocephala (Vieillot, 1818) X   X       X      X    X   X   FM   SF Euphonia pectoralis (Latham, 1801)E X    X X   X       X X         D   SF Chlorophonia cyanea (Thunberg, 1822) X                     X   I   SF Estrildidae                              Estrilda astrild (Linnaeus, 1758) X                     X   S   SE Passeridae                             Passer domesticus (Linnaeus, 1758) X                       S   EO APPENDIX II Species found in literature review and not included in the final list (Appendix I), since they were recorded only once and could represent dubious records or because their distributional ranges do not include northern Paraná state. Nomenclature of species follows Piacentini et al. (2015). Species Literature Trogon viridis Linnaeus, 1766 Anjos et al. 1997, Anjos 2001 Cyanerpes cyaneus (Linnaeus, 1766) Anjos et al. 1997 Attila rufus (Vieillot, 1819) Anjos et al. 1997 Dysithamnus stictothorax (Temminck, 1823) Anjos et al. 1997, Anjos et al. 2004 Drymophila ferruginea (Temminck, 1822) Anjos et al. 1997, Anjos et al. 2004 Hemitriccus nidipendulus (Wied, 1831) Anjos et al. 1997 Phylloscartes oustaleti (Sclater, 1887) Anjos et al. 1997 Saltatricola atricollis (Vieillot, 1817) Anjos et al. 1997 Aramides cajaneus (Statius Muller, 1776) Anjos et al. 2007 Anabacerthia amaurotis (Temminck, 1823) Anjos et al. 2007 Patagioenas maculosa (Temminck, 1813) Bochio & Anjos 2012 Cichlocolaptes leucophrus (Jardine & Selby, 1830) Bochio & Anjos 2012 Campylorhamphus trochilirostris (Lischtenstein, 1820) Bochio & Anjos 2012

Journal

Ornithology ResearchSpringer Journals

Published: Sep 1, 2016

Keywords: avifauna; Atlantic Forest; forest fragment dynamism; Protected Area; species persistence

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