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Bird mortality due to collisions in glass panes on an Important Bird Area of southeastern Brazil

Bird mortality due to collisions in glass panes on an Important Bird Area of southeastern Brazil Revista Brasileira de Ornitologia 25(2): 90 0 0–101. ARTICLE June 2017 Bird mortality due to collisions in glass panes on an Important Bird Area of southeastern Brazil 1,2,3 1 1 Lucas Penna Soares Santos , Vinícius Ferreira de Abreu & Marcelo Ferreira de Vasconcelos Museu de Ciências Naturais, Pontifícia Universidade Católica de Minas Gerais. Avenida Dom José Gaspar, 290, Bairro Coração Eucarístico, 30535-901, Belo Horizonte, MG, Brazil. Programa de Pós-graduação em Biologia de Vertebrados, Pontifícia Universidade Católica de Minas Gerais. Avenida Dom José Gaspar, 500, Bairro Coração Eucarístico, 30535-610, Belo Horizonte, MG, Brazil. Corresponding author: penna.lucas@gmail.com Received on 14 February 2017. Accepted on 22 June 2017. ABSTRACT: Human-caused alterations to the environment are important causes of the loss of bird biodiversity globally. Collisions with windows are the second leading human cause of mortality for birds, and it is estimated that 100 million to one billion birds die due to window collisions annually in the US alone. However, in Brazil there have been no systematic studies on bird mortality due to collisions with man-made structures. Our aims with this study were to record the bird species that died due to collisions with windows in an Important Bird Area of southeastern Brazil, accessing the eff ects of species characteristics (forest dependence, wing type, threaten status, endemism, migratory habits) and climatic seasonality on bird-window collisions. Dead birds were collected daily during 2010 to 2013 and occasional records were obtained from 2000–2009 and 2014–2015 in Reserva Particular do Patrimônio Natural Santuário do Caraça, Minas Gerais, southeastern Brazil. We found 168 birds individuals of 57 species dead due to collisions against windows. Individuals classifi ed as forest dependent and with elliptical type wings were the most common among birds dead due to collisions. There was no difference between the number of dead individuals in the dry and rainy seasons, and rainfall was not correlated with bird collisions. Th e occurrence of threatened, endemic and migrant species in our sample demonstrates the importance to continue this type of research in Brazil and other localities throughout the Neotropics. Our data can support studies that investigate the influence of other factors and characteristics of natural history of bird collisions, particularly in areas with similar man-made structures as at our study site. KEY-WORDS: bird collisions, mortality, natural history, RPPN Santuário do Caraça, seasonality. INTRODUCTION each species and their biological characteristics (Bevanger 1994). Th e magnitude of the problem is so signifi cant that Human activities can negatively alter natural regions major changes in the ecology and behavior of birds have been reported (Johnson et al. 2002), especially regarding and biological systems, as has been recently discussed in many reports and environmental impact analyses of wild migratory species (Rybak et al. 1973, Klem-Jr. 1990a, communities (Loss et al. 2012). Such human interference b, Erickson et al. 2001, 2005, Manville 2001, Diehl can cause significant dama ge, especially among birds (e.g. et al. 2014). Some examples include changes in fl ight Bevanger 1994, Piorkowski 2006, Johnson et al. 2002, routes and lower fli ght altitudes caused by an increase in obstacles such as wind farms and electric transmission Drewitt & Langston 2008), due to their diversity and their frequent cohabitation with humans in a variety of towers (Winkelman 1995, Leddy et al. 1999, Borden et environments (Le Corre et al. 2009, Ryder et al. 2012). al. 2010). Collisions with man-made structures are the second Some studies have related the characteristics of greatest source of human-caused bird mortality worldwide particular bird species with human impacts. For example, forest dependent species are more susceptible to negative (Klem-Jr. 2008). Such incidents have been documented globally (Avery et al. 1978, Avery 1979, Klem-Jr. 1990a, changes in the environment (Marini 2001, Maldonado- Morrinson 1998, Erickson et al. 2001, 2005, Veltri & Klem- Coelho & Marini 2003, Roma 2006, Ramos et al. Jr. 2005, Hager et al. 2008) and represent an important 2011). Maneuverability, including wing type and fl ight source of negative anthropic influence on nature (Banks speed, of each species relates to fl ight behavior and thus collisions risk (APLIC 2012, Sporer et al. 2013). Thus, 1979, Drewitt & Langston 2006, 2008). Th e vulnerability to human impacts and the slow-fl ying or walking birds do not cover large areas and potential risk of bird collision is related differently for thus are less prone to collisions than long-distance or fast- Revista Brasileira de Ornitologia 25(2): 2017 Bird mortality due to collisions in glass panes Santos et al. flying species (Klem-Jr. 1989, Bevanger 1994). Lastly, southeastern Brazil, is a private reserve with 11,233 ha seasonal and weather conditions have been reported (Santuário do Caraça 2013), in the Quadrilátero Ferrífero to influence variation in the annual number of bird (Iron Quadrangle) region in the southern portion of collisions (Bevanger 1994, Drewitt & Langston 2008). the Serra do Espinhaço (Espinhaço Mountain Range; For example, the collision frequency is directly related to Fig. 1). The region lies within the Atlantic Forest the increase in rainfall, which generally coincides with domain, yet close to the Cerrado domain, two world hotspots of biodiversity (Myers et al. 2000, Vasconcelos the reproductive period in southeastern Brazil (Marini & Durães 2001), and is a function of foraging and other 2000). A very heterogeneous vegetation and different biological activities, as well as reduced visibility (Gabrey phytophysiognomies are found in RPPNSC, such as high & Doolber 1996, Steele 2001). altitude rocky fields ( campos rupestres s), semideciduous Studies of bird collisions are usually conducted in and cloud forests (Mota 2006). In contrast, historically, urban, suburban or rural environments and rarely in this protected area suffers anthropic pressure in its protected areas or regions that have been identified as surroundings, such as mining and farming, interrupting important conservation areas (Klem-Jr. 2008, Gelb & the landscape connectivity, with others protected and Delacretaz 2009). Important Bird Areas (IBAs) represent natural areas (Vasconcelos 2013). a global network of important sites for the conservation The climate of RPPNSC is seasonal , with well- of birds and biodiversity. Worldwide, 12,000 IBAs defined dry (April to September) and rainy (October to have been identifi ed, with 234 IBAs mapped in Brazil, March) seasons, with mild mean annual temperatures where endemic and threatened species occur (Develey & (18–19°C) and low (0°C or less) temperatures mainly at Goerck 2009, BirdLife International 2014). Nevertheless, higher elevations (Dutra et al. 2002). The Köppen-Gei ger several problems have been reported regarding human climatological classifi cation defi nes this area as Cwb interference in areas devoted to conservation, for example, (humid temperate climate with dry winters and temperate exploration of land use in surroundings, fragmentation, summers, similar to tropical climate of altitude) (Alvares et al. 2013) and the annual average rainfall is above 1500 wildfi res and ineff ective surveillance (Lima et al. 2005, Rylands & Brandon 2005). mm. Records for bird collisions with aircraft, power lines In the area 372 bird species had been recorded, and vehicles have been increasing in Brazil, but there including 13 threatened species, 75 migrants, 74 Atlantic remains much to be understood about this phenomenon Forest endemics, four Cerrado endemics and four species restricted to mountain-tops of southeastern Brazil (Nascimento et al. 2005, Laurance et al. 2009, Rosa & Bager 2012). Only a few studies have focused on bird (Chesser 1994, Vasconcelos 2013). Serra do Caraça has mortality due to collisions with man-made structures in one of the richest avifaunas of eastern Brazil, it is an Brazil (ACS 2006, Carrano 2006, Muhlenberg College important area for bird conservation on both regional and 2009, Santos et al. 2011, Soares et al. 2011, Stolk et global scales (Vasconcelos & Melo-Júnior 2001, Bencke et al. 2006, Develey & Goerck 2009). Th e area is located al. 2015), making it difficult to make comparisons and determine influential factors. This is particularly true in an IBA (BR145; BirdLife International 2009, 2012, given the great bird diversity of Brazil and the large size Develey & Goerck 2009), an Endemic Bird Area (EBA of the country, thereby confounding attempts to develop 073; Stattersfield et al. 1998) and a Biosphere Reserve preventive measures or findin g solutions. (UNESCO 2005). In this paper, we report on bird collisions with windows in a Brazilian protected area and IBA, considering Data collection characteristics such as forest dependence, wing type, threaten status, endemism and migratory habits of each Th e RPPNSC is locally well known for its historical man- species. We also tested for a seasonal relationship between made architecture. One of the buildings is the Caraça Museum (Fig. 1), which is 70 m nearly from the forested seasons (dry and rainy) and the number of dead birds. vegetation and has sides that comprised large, reflective tempered glass windows (Fig. 2). On those windows METHODS (408.5 m ) occur bird collisions under investigation in the present study. Study area Dead birds were collected daily, but stored in freezer by monthly lots, during 2010 to 2013, with Th e Reserva Particular do Patrimônio Natural Santuário do the assistance of the environmental team of RPPNSC. o o Caraça a (hereafter RPPNSC - 20 05'51"S; 43 29'18"W; Additional casual non-systematic records were carried out elevation 1290 m a.s.l.), located in the municipalities during 2000–2009 and 2014–2015. Specimens found of Catas Altas and Santa Bárbara, state of Minas Gerais, dead were placed in individual plastic bags with a label Revista Brasileira de Ornitologia 25(2): 2017 Bird mortality due to collisions in glass panes Santos et al. R R R R R R R :  :  :  :  : R R Figure 1. Location map ( ( (A A A) and aerial image of the Reserva Particular do Patrimônio Natural Santuário do Caraça, showing the architectural complex (B). The dark grey box is the Caraça Museum with sides ( ( (A–D) comprised of windows. P P Figure 2. Architectural sketch of Caraça Museum showing the details of the building and the width, height and depth of its sides. Percentage and area (in m ) of glass (grey areas) on each side of the Caraça Museum: ( ( (A A A)  31% (110); (B)  90% (151.5); (C) 34.9% (124.2); (D)  13.6% (22.8). Revista Brasileira de Ornitologia 25(2): 2017 Bird mortality due to collisions in glass panes Santos et al. dead from collision between the two seasons (dry and containing basic collection data and frozen. Specimens rainy) we used the Shapiro-Wilk test for normality were deposited (mostly as study skins and/or skeletons) in and, subsequently, t t t-test for two independent samples the following collections: Museu de Ciências Naturais da (parametric). The F F F-test was used to compare sample Pontifícia Universidade Católica de Minas Gerais (MCNA), distributions of the two seasons. We analyzed the Department of Zoology of the Universidade Federal de seasonality only for specimens for which the month of Minas Gerais (DZUFMG) and Museu de Zoologia da their collision was known. A rate per day (the number of Universidade de São Paulo (MZUSP). We identified all collided birds by the total of days in each season) was used individuals to species level following nomenclature in for comparison between the systematic sampling periods. Piacentini et al. (2015). Using monthly rainfall (in mm) at RPPNSC during 2010–2013, we assessed diff erences in rainfall for each Data analysis season using factorial ANOVA. To evaluate rainfall as a factor of bird mortality, we performed a Pearson product We classified the s pecimens qualitatively and moment correlation between average monthly rainfall and quantitatively for attributes from the literature: I) Forest number of individuals found dead from collision. dependence (Silva 1995, Parker-III et al. 1996): 1) independent (species that occur in open vegetation), 2) Statistical analyses were conducted in R Software (R Core Team 2017;  = 0.05) and used all birds found dead semi-dependent (species that occur in open vegetation as a result of colliding with the windows of the Caraça and forest), and 3) dependent (species found mainly in forest habitats); II) Wing types (Scott & McFarland Museum. Plotrix package v. 3.6-1 (Lemon et alll. 2015) was used for producing the radial graph. 2010): 1) elliptical, 2) game bird, 3) high-aspect ratio, 4) high-speed, and 5) slotted high-lift; III) Th reat status: 1) global (IUCN 2015), 2) national (MMA 2014a, b), and RESULTS 3) state (COPAM 2010); IV) Endemism: 1) Cerrado (Silva 1995), 2) Atlantic Forest (Brooks et al. 1999) and 3) mountaintops of eastern Brazil (Vasconcelos 2008); A total of 168 specimens of 57 species (Appendix I) were found dead presumably due to collisions with glass panes and V) Migration: austral migrants (sensu Chesser 1994). of the Caraça Museum. Th e mortality rates for the period To test for significant differences in the proportions of systematic sampling (102 individuals in 2010–2013) were of  2.12 deaths/month and 25.50 deaths/year. of collided birds among categories of forest dependence and wing types, we use separate Chi-Square tests with no Th e orders most aff ected were Passeriformes diff erence among categories as the expected proportion. (102 individuals) and Columbiformes (44) (Table 1). Regarding families, the most affected were Columbidae We also performed Partition Likelihood Ratio Chi- Square to evaluate relationships between categories of (44 individuals), Thrau pidae (35), Trochilidae (16) and both of these characteristics. Hirundinidae (15), whereas the most affected genera To test for diff erences in the number of birds were Turdus s (13) and Tangara a (11). The most commonly Table 1. Orders of birds dead due to collisions with windows of the Caraça Museum, Minas Gerais state, Brazil, and the number of individuals for each category of forest dependence and wing type. Dependent 2 1 41 0 9 0 0 44 97 Semi-dependent 0 0 3 1 6 1 1 27 39 Independent 0 0 0 0 1 0 0 31 32 Elliptical 0 1 44 0 0 1 0 87 133 High-speed 0 0 0 1 16 0 0 15 32 Slotted 0 0 0 0 0 0 1 0 1 Game Bird 2 0 0 0 0 0 0 0 2 Total 2 1 44 1 16 1 1 102 168 Revista Brasileira de Ornitologia 25(2): 2017 Galiiformes Accipritiformes Columbiformes Psitaciformes Apodiformes Coraciiformes Piciformes Passeriformes Total Bird mortality due to collisions in glass panes Santos et al. encountered species were the Plumbeous Pigeon (Patagioenas plumbea) (35 individuals) and the Blue-and- white Swallow (Pygochelidon cyanoleuca) (13). We found greater mortality for forest dependent (97 individuals; 57.8%) and semi-dependent (39; 23.2%) species than independent species (32; 19.0%). Forest dependence had the greatest influence on bird mortalit y ( = 46.46; P < 0.0001). Among wing types, species classified as having elliptical wings were the most affected (133 individuals; 79.2%), followed by high-speed (32; 19%), game bird (2; 1.2%) and slotted high-lift (1; 0.6%) wings. Elliptical wings diff ered signifi cantly from the other categories of wing types ( = 277.67; P < 0.0001). The interaction between the natural history characteristics of forest dependence and wing type had a significant general value (Table 2). A significant diff erence was found for partition one ( = 24.11; 2×3 tables P = 0.0001), demonstrating that individuals classified as Fi Figure 3 3. R Radi diall graph h of f th he average numb ber of f i indi divid idualls forest dependent with elliptical wings are more frequently found dead in each month of the two study seasons (polygon; light grey: dry season; dark grey: rainy season; grid scale: 0–14). aff ected by collisions. Data points (in black) and respective numbers reveal the average In relation to threaten status, only two species monthly rainfall (mm) for 2010–2013 in RPPN Santuário do were considered globally “Near Th reatened”: the Caraça a (grid scale: 0–700). Hyacinth Visorbearer Augastes scutatus s (1 individual) and the Swallow-tailed Cotinga Phibalura flavirostris s (2 individuals); the latter is also considered “Vulnerable” DISCUSSION in the state of Minas Gerais. All other specimens were classifi ed as “Least Concern” species at the global, national Sixteen percent of the total number of bird species known and/or state levels. to occur in RPPNSC was aff ected by collisions with the Endemic species were represented by 38 specimens of studied structure. However, it is important to stress that, the Atlantic Rain Forest and one (Hyacinth Visorbearer) even with the helpful assistance of the environmental from the mountains of eastern Brazil. Twenty-seven individuals of 10 species of austral migrants were found team of the reserve, it is possible that several dead specimens were overlooked. Specimens may have been dead by collisions throughout our study. missed due to their rapid decomposition due to natural No significant seasonal mortality pattern was found factors such as weather, sunlight, rain, necrophagous between the rainy (44 individuals; rate [collided birds/ animals (invertebrates such as ants, fl ies, beetles) and rainy days] = 16.56) and dry (54; rate [collided birds/ dry days] = 13.55) seasons (t t = 0.96; P P = 0.362; F F = 1.01; other biological agents (bacterial digestion) (Crawford 1971, Balcomb 1986, Pain 1991, Wobeser & Wobeser P P = 0.99) (Fig. 3). The significant difference in monthly 1992). Scavengers and opportunist vertebrate predators rainfall between the seasons (F F F(seasons) = 37.44; P < also can remove small bird carcasses within a matter of a 0.0001) was not correlated with bird mortality. Table 2. Number of individuals dead due to collisions with windows of the Caraça Museum, Minas Gerais state, Brazil, classifi ed by category of interaction between forest dependence and wing type. Categories Dependent Semi-dependent Independent Elliptical 86 31 16 High-speed 9 7 16 Game bird 2 0 0 Slotted high-lift 0 1 0 Chi-square value 30.295 Significance level P P < 0.0001 Revista Brasileira de Ornitologia 25(2): 2017 Bird mortality due to collisions in glass panes Santos et al. few minutes after death and it is also believed that many Columbiformes, can be related with the susceptible when collisions may not result in immediate death, which may they cross open environments and other characteristics, imply that most of the studies on bird mortality due such as photophobia and forest proximity. to human factors are underestimates (Klem-Jr. 1990a, Sporer et al. (2013) noted that high-speed and Morris 2002, Antworth et al. 2005, Kummer et al. 2016). elliptical-winged birds frequently collide with power Forest dependent birds were most frequently aff ected lines. High-speed birds were represented in our sample by collisions in RPPNSC. We interpret this as the Caraça by some species of Trochilidae and Hirundinidae, which Museum building disrupts a natural corridor formed not only possess fast flight, but also can remain in by the surrounding vegetation, and forest birds fail to flight for a greater period of time (Scott & McFarland recognize this obstacle as a change of habitat. In contrast, 2010). Jenkins et al. (2010) pointed out that high speed the lower number of forest independent species can be affects the reaction time of bir ds to avoid collisions with attributed to their ability to recognize edges in open areas, anthropic structures. Game birds, which generally have since these species should have a better perception of slotted and high-aspect wing types, were not abundant in obstacles, and thus be more able to avoid them. our sample, and exhibit other fli ght performances such as In general, forest dependent species react more soaring, lift and difficult take-offs. negatively to environmental changes than forest The frequency of collisions with the large windows independent species. For example, the presence of forests of the Caraça Museum can be evaluated in the context next to roads increased roadkill of forest species (Marini of the surrounding landscape and thus the reflections o f 2001, Ramos et al. 2011). Although it is known that the vegetation in the windows (Ogden 1996, Gelb & forest birds avoid crossing large open areas (Grubb-Jr. & Delacretaz 2009, Klem-Jr. 2009). Th e Caraça Museum is Doherty-Jr. 1999, Develey & Stouff er 2001), these species adjacent to a large forested area, but is situated in an open perform frequent movements in their environments space inside the architectural complex. Sensory analyses and may cross-forest fragments, especially those species have determined that birds perceive such reflections adapted to patchy environments (Marini 2001, Yabe et as an extension of the physical environment, and their al. 2010). visual system is not exclusively dedicated to perceiving The hi gh incidence of collisions by native pigeons fi xed obstacles, such as human structures, thus eventually (Columbidae), especially the Plumbeous Pigeon, leading to collisions with windows (Martin & Shaw signifi cantly infl uenced the interpretation of our analysis. 2010, Martin 2011). Perhaps the abundance of this species in RPPNSC, and Our data did not show any seasonal diff erence in bird the patterns of its biological activities, such as feeding, mortality between dry and rainy seasons. Th e RPPNSC dispersal and reproduction are responsible for the experiences high variation in monthly rainfall, but slight high collision rate of this species. In conjunction, the oscillations in other abiotic factors such as temperature abundance and differential use of s pecific habitats b y and wind speed and direction, as has been reported bird populations is also of fundamental importance to previously (Moreira & Pereira 2013). A relationship predicting collisions (De Lucas et al. 2008, Marques et between bird collisions with artifi cial structures and al. 2014). Other studies also report a high incidence of seasonal patterns can be more important in regions where accidents with Columbidae species, including birdstrikes climate conditions exhibit larger variations, but is also on aircrafts and windows collisions (Dolbeer 2006, related to routes and additional types of migrant species Kitowski 2011, Ocampo-Peñuela et al. 2016). (e.g. Klem-Jr. 1989, Borden et alll. 2010). Diff erent wing types are associated with diff erent Other weather and meteorological factors, such as fli ght performances (Warham 1977, Copete 1999). In daily temperature, air humidity, sunlight, clouds and the case of power lines, fl ight behavior is one of the most mist, change the perception of, and interaction with, important biological features for bird collisions (Bevanger the physical environmental by birds (e.g. Bevanger 1994, Janss 2000). Th e prominent number of collisions 1994, Drewitt & Langston 2008, Martin 2011). In the by birds with elliptical wings in the present study indicates Neotropical region, the infl uence of these conditions on that birds with this characteristic have a greater tendency bird collisions is still unknown, and there certainly are for collisions. Scott and McFarland (2010) explain that other environmental factors shaping this interaction, birds with elliptical wings have quick bursts of speed and such as changes in the composition of food resources or are most adept at navigating densely vegetated habitats. patterns of other biological activities. Further exploration This fact contextualizes the hi gh representation of this of seasonal patterns of birds may help to uncover category in our sample, especially due to the proximity fundamental answers about bird collisions, and provide of vegetation to the Caraça Museum. Further, the strong important information for strategies to mitigate this association of elliptical wings and forest dependent birds, problem (Borden et alll. 2010). which the most represented orders were Passeriformes and It is important to stress that all bird species are not Revista Brasileira de Ornitologia 25(2): 2017 Bird mortality due to collisions in glass panes Santos et al. of scavenging on estimates of roadkilled vertebrates. Southeastern equally susceptible to mortality by collisions (Bevanger Naturalist t 4: 647–656. 1994, Drewitt & Langston 2008, Loss et al. 2014). APLIC (Avian Power Line Interaction Committee). 2012. Reducing Borden et al. (2010) mention that bird collisions are a avian collisions with power lines: the state of the art in 2012. complex question and there are no simple relationships Washington: Edison Electric Institute and Avian Power Line that explain it in its entirety. Furthermore, species Interaction Committee. Avery M.L. 1979. 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APPENDIX I List of species found dead due to collisions with the Caraça Museum (RPPN Santuário do Caraça) and their respective data, as follow: Forest dependence: D - Dependent; S - Semi-dependent and; I - Independent; Wing type: E - Elliptical; HS - High-Speed; ST - Slotted; GB - Game Bird; Conservation Status: LC - Least Concern; NT - Near G N S Th reatened; Globally Level; National Level; State Level; Seasonality: month of collision (number of individuals AF MT M that collided); Atlantic Rain Forest Endemism; Mountaintops of Southeastern Brazil Endemism; Migratory species. Taxon Cracidae Rafi nesque, 1815 Dusky-legged Guan G, N, S 2 D GB LC 2 (1), 4 (1) Penelope obscura Temminck, 1815 Accipitridae Vigors, 1824 Bicolored Hawk G, N, S 1 D E LC - Accipiter bicolor (Vieillot, 1817) Columbidae Leach, 1820 Blue Ground-Dove G, N, S 1 S E LC 11 (1) Claravis pretiosa (Ferrari-Perez, 1886) Plumbeous Pigeon 1 (4), 2 (2), 4 (2), 5 (1), G, N, S 35 D E LC Patagioenas plumbea (Vieillot, 1818) 6 (1), 9 (1), 12 (2) White-tipped Dove G, N, S 2 S E LC 1 (1) Leptotila verreauxi Bonaparte, 1855 Gray-fronted Dove G, N, S 4 D E LC 4 (2) Leptotila rufaxilla (Richard & Bernard, 1792) Ruddy Quail-Dove G, N, S 2 D E LC 6 (1), 9 (1) Geotrygon montana (Linnaeus, 1758) Psittacidae Rafines que, 1815 White-eyed Parakeet G, N, S 1 S HS LC - Psittacara leucophthalmus s (Statius Muller, 1776) Trochilidae Vigors, 1825 Planalto Hermit G, N, S 1 S HS LC - Phaethornis pretrei i (Lesson & Delattre, 1839) AF Scale-throated Hermit G, N, S 1 D HS LC 7 (1) Phaethornis eurynome (Lesson, 1832) White-vented Violetear G, N, S 1 S HS LC 4 (1) Colibri serrirostris s (Vieillot, 1816) Glittering-bellied Emerald G, N, S 3 S HS LC 3 (1) Chlorostilbon lucidus s (Shaw, 1812) AF Violet-capped Woodnymph G, N, S 1 D HS LC 7 (1) Thalurania glaucopis (Gmelin, 1788) Versicolored Emerald G, N, S 1 D HS LC 10 (1) Amazilia versicolor (Vieillot, 1818) Sapphire-spangled Emerald G, N, S 3 D HS LC 4 (1), 6 (1), 7 (1) Amazilia lactea (Lesson, 1832) AF Brazilian Ruby G, N, S 3 D HS LC 10 (1) Heliodoxa rubricauda (Boddaert, 1783) MT Hyacinth Visorbearer G N, S 1 I HS NT ; LC 4 (1) Augastes scutatus (Temminck, 1824) Amethyst Woodstar G, N, S 1 S HS LC - Calliphlox amethystina (Boddaert, 1783) Revista Brasileira de Ornitologia 25(2): 2017 Number of individual Forest dependence Wing type Conservation status Seasonality Bird mortality due to collisions in glass panes Santos et al. Taxon Alcedinidae Rafinesque, 1815 Green Kingfisher G, N, S 1 S E LC 1 (1) Chloroceryle americana (Gmelin, 1788) Ramphastidae Vigors, 1825 Toco Toucan G, N, S 1 S ST LC - Ramphastos toco Statius Muller, 1776 Thamnophilidae Swainson, 182 4 AF Large-tailed Antshrike G, N, S 1 D E LC 7 (1) Mackenziaena leachii (Such, 1825) Furnariidae Gray, 1840 Rufous Hornero G, N, S 1 I E LC - Furnarius rufus s (Gmelin, 1788) AF Pallid Spinetail G, N, S 2 D E LC 2 (1), 8 (1) Cranioleuca pallida (Wied, 1831) Pipridae Rafines que, 1815 AF Serra do Mar Tyrant-Manakin G, N, S 1 D E LC 9 (1) Neopelma chrysolophum Pinto, 1944 White-bearded Manakin G, N, S 1 D E LC 5 (1) Manacus manacus (Linnaeus, 1766) AF Pin-tailed Manakin G, N, S 2 D E LC 9 (1) Ilicura militaris (Shaw & Nodder, 1809) AF Swallow-tailed Manakin G, N, S 4 D E LC 4 (1), 5 (1), 6 (1) Chiroxiphia caudata (Shaw & Nodder, 1793) Tityridae Gray, 1840 White-winged Becard G, N, S 1 S E LC 9 (1) Pachyramphus polychopterus (Vieillot, 1818) Cotingidae Bonaparte, 1849 M G N Swallow-tailed Cotinga NT ; LC ; 2 D E 11 (1) Phibalura flavirostri s Vieillot, 1816 VU Rhynchocyclidae Berlepsch, 1907 AF Gray-hooded Flycatcher G, N, S 5 D E LC 6 (2), 11 (1) Mionectes rufi ventris Cabanis, 1846 AF Hangnest Tody-Tyrant G, N, S 2 S E LC 6 (2) Hemitriccus nidipendulus (Wied, 1831) Tyrannidae Vigors, 1825 Great Kiskadee G, N, S 2 I E LC - Pitangus sulphuratus (Linnaeus, 1766) AF Velvety Black-Tyrant G, N, S 6 S E LC 5 (1), 6 (2) Knipolegus nigerrimus (Vieillot, 1818) Hirundinidae Rafinesque, 181 5 Blue-and-white Swallow G, N, S 13 I HS LC 1 (3), 10 (1), 12 (4) Pygochelidon cyanoleuca (Vieillot, 1817) Southern Rough-winged Swallow G, N, S 2 I HS LC - Stelgidopteryx rufi collis (Vieillot, 1817) Turdidae Rafinesque, 181 5 Yellow-legged Thrush G, N, S 3 D E LC 4 (1) Turdus flavipes Vieillot, 1818 Pale-breasted Thrus h G, N, S 1 S E LC - Turdus leucomelas Vieillot, 1818 Rufous-bellied Thrus h G, N, S 2 I E LC 12 (1) Turdus rufi ventris Vieillot, 1818 Revista Brasileira de Ornitologia 25(2): 2017 Number of individual Forest dependence Wing type Conservation status Seasonality Bird mortality due to collisions in glass panes Santos et al. Taxon Creamy-bellied Thrush G, N, S 2 S E LC 10 (2) Turdus amaurochalinus Cabanis, 1850 White-necked Thrus h G, N, S 5 D E LC 7 (1), 8 (1), 12 (1) Turdus albicollis Vieillot, 1818 Passerellidae Cabanis & Heine, 1850 Rufous-collared Sparrow G, N, S 1 I E LC 1 (1) Zonotrichia capensis s (Statius Muller, 1776) Icteridae Vigors, 1825 Red-rumped Cacique G, N, S 2 S E LC 2 (1), 11 (1) Cacicus haemorrhous (Linnaeus, 1766) Shiny Cowbird G, N, S 1 I E LC - Molothrus bonariensis s (Gmelin, 1789) Th raupidae Cabanis, 1847 Cinnamon Tanager G, N, S 1 I E LC 11 (1) Schistochlamys rufi capillus (Vieillot, 1817) Sayaca Tanager 2 (1), 8 (1), 9 (1), 10 G, N, S 6 S E LC Tangara sayaca (Linnaeus, 1766) (1) Palm Tanager G, N, S 1 S E LC 8 (1) Tangara palmarum (Wied, 1821) AF Golden-chevroned Tanager G, N, S 2 D E LC 2 (1) Tangara ornata (Sparrman, 1789) Burnished-buff Tanager G, N, S 2 I E LC - Tangara cayana (Linnaeus, 1766) Saff ron Finch G, N, S 3 I E LC - Sicalis flaveolaa (Linnaeus, 1766) AF Uniform Finch G, N, S 4 D E LC 4 (1), 7 (1), 12 (1) Haplospiza unicolor Cabanis, 1851 AF Black-goggled Tanager G, N, S 1 D E LC 8 (1) Trichothraupis melanops (Vieillot, 1818) AF Ruby-crowned Tanager G, N, S 4 D E LC 4 (1), 8 (1), 9 (1) Tachyphonus coronatus (Vieillot, 1822) Swallow Tanager G, N, S 1 D E LC 4 (1) Tersina viridis (Illiger, 1811) Blue Dacnis G, N, S 5 S E LC 7 (1) Dacnis cayana a (Linnaeus, 1766) Sporophila a sp. 2 I E - 1 (1) Yellow-bellied Seedeater G, N, S 1 I E LC 7 (1) Sporophila nigricollis (Vieillot, 1823) Green-winged Saltator G, N, S 1 S E LC - Saltator similis s d'Orbigny & Lafresnaye, 1837 Fringillidae Leach, 1820 Blue-naped Chlorophonia G, N, S 6 D E LC 3 (1), 6 (1), 7 (1) Chloroppy honia cyanea (Thunber g g, 1822) Revista Brasileira de Ornitologia 25(2): 2017 Number of individual Forest dependence Wing type Conservation status Seasonality http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Ornithology Research Springer Journals

Bird mortality due to collisions in glass panes on an Important Bird Area of southeastern Brazil

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Revista Brasileira de Ornitologia 25(2): 90 0 0–101. ARTICLE June 2017 Bird mortality due to collisions in glass panes on an Important Bird Area of southeastern Brazil 1,2,3 1 1 Lucas Penna Soares Santos , Vinícius Ferreira de Abreu & Marcelo Ferreira de Vasconcelos Museu de Ciências Naturais, Pontifícia Universidade Católica de Minas Gerais. Avenida Dom José Gaspar, 290, Bairro Coração Eucarístico, 30535-901, Belo Horizonte, MG, Brazil. Programa de Pós-graduação em Biologia de Vertebrados, Pontifícia Universidade Católica de Minas Gerais. Avenida Dom José Gaspar, 500, Bairro Coração Eucarístico, 30535-610, Belo Horizonte, MG, Brazil. Corresponding author: penna.lucas@gmail.com Received on 14 February 2017. Accepted on 22 June 2017. ABSTRACT: Human-caused alterations to the environment are important causes of the loss of bird biodiversity globally. Collisions with windows are the second leading human cause of mortality for birds, and it is estimated that 100 million to one billion birds die due to window collisions annually in the US alone. However, in Brazil there have been no systematic studies on bird mortality due to collisions with man-made structures. Our aims with this study were to record the bird species that died due to collisions with windows in an Important Bird Area of southeastern Brazil, accessing the eff ects of species characteristics (forest dependence, wing type, threaten status, endemism, migratory habits) and climatic seasonality on bird-window collisions. Dead birds were collected daily during 2010 to 2013 and occasional records were obtained from 2000–2009 and 2014–2015 in Reserva Particular do Patrimônio Natural Santuário do Caraça, Minas Gerais, southeastern Brazil. We found 168 birds individuals of 57 species dead due to collisions against windows. Individuals classifi ed as forest dependent and with elliptical type wings were the most common among birds dead due to collisions. There was no difference between the number of dead individuals in the dry and rainy seasons, and rainfall was not correlated with bird collisions. Th e occurrence of threatened, endemic and migrant species in our sample demonstrates the importance to continue this type of research in Brazil and other localities throughout the Neotropics. Our data can support studies that investigate the influence of other factors and characteristics of natural history of bird collisions, particularly in areas with similar man-made structures as at our study site. KEY-WORDS: bird collisions, mortality, natural history, RPPN Santuário do Caraça, seasonality. INTRODUCTION each species and their biological characteristics (Bevanger 1994). Th e magnitude of the problem is so signifi cant that Human activities can negatively alter natural regions major changes in the ecology and behavior of birds have been reported (Johnson et al. 2002), especially regarding and biological systems, as has been recently discussed in many reports and environmental impact analyses of wild migratory species (Rybak et al. 1973, Klem-Jr. 1990a, communities (Loss et al. 2012). Such human interference b, Erickson et al. 2001, 2005, Manville 2001, Diehl can cause significant dama ge, especially among birds (e.g. et al. 2014). Some examples include changes in fl ight Bevanger 1994, Piorkowski 2006, Johnson et al. 2002, routes and lower fli ght altitudes caused by an increase in obstacles such as wind farms and electric transmission Drewitt & Langston 2008), due to their diversity and their frequent cohabitation with humans in a variety of towers (Winkelman 1995, Leddy et al. 1999, Borden et environments (Le Corre et al. 2009, Ryder et al. 2012). al. 2010). Collisions with man-made structures are the second Some studies have related the characteristics of greatest source of human-caused bird mortality worldwide particular bird species with human impacts. For example, forest dependent species are more susceptible to negative (Klem-Jr. 2008). Such incidents have been documented globally (Avery et al. 1978, Avery 1979, Klem-Jr. 1990a, changes in the environment (Marini 2001, Maldonado- Morrinson 1998, Erickson et al. 2001, 2005, Veltri & Klem- Coelho & Marini 2003, Roma 2006, Ramos et al. Jr. 2005, Hager et al. 2008) and represent an important 2011). Maneuverability, including wing type and fl ight source of negative anthropic influence on nature (Banks speed, of each species relates to fl ight behavior and thus collisions risk (APLIC 2012, Sporer et al. 2013). Thus, 1979, Drewitt & Langston 2006, 2008). Th e vulnerability to human impacts and the slow-fl ying or walking birds do not cover large areas and potential risk of bird collision is related differently for thus are less prone to collisions than long-distance or fast- Revista Brasileira de Ornitologia 25(2): 2017 Bird mortality due to collisions in glass panes Santos et al. flying species (Klem-Jr. 1989, Bevanger 1994). Lastly, southeastern Brazil, is a private reserve with 11,233 ha seasonal and weather conditions have been reported (Santuário do Caraça 2013), in the Quadrilátero Ferrífero to influence variation in the annual number of bird (Iron Quadrangle) region in the southern portion of collisions (Bevanger 1994, Drewitt & Langston 2008). the Serra do Espinhaço (Espinhaço Mountain Range; For example, the collision frequency is directly related to Fig. 1). The region lies within the Atlantic Forest the increase in rainfall, which generally coincides with domain, yet close to the Cerrado domain, two world hotspots of biodiversity (Myers et al. 2000, Vasconcelos the reproductive period in southeastern Brazil (Marini & Durães 2001), and is a function of foraging and other 2000). A very heterogeneous vegetation and different biological activities, as well as reduced visibility (Gabrey phytophysiognomies are found in RPPNSC, such as high & Doolber 1996, Steele 2001). altitude rocky fields ( campos rupestres s), semideciduous Studies of bird collisions are usually conducted in and cloud forests (Mota 2006). In contrast, historically, urban, suburban or rural environments and rarely in this protected area suffers anthropic pressure in its protected areas or regions that have been identified as surroundings, such as mining and farming, interrupting important conservation areas (Klem-Jr. 2008, Gelb & the landscape connectivity, with others protected and Delacretaz 2009). Important Bird Areas (IBAs) represent natural areas (Vasconcelos 2013). a global network of important sites for the conservation The climate of RPPNSC is seasonal , with well- of birds and biodiversity. Worldwide, 12,000 IBAs defined dry (April to September) and rainy (October to have been identifi ed, with 234 IBAs mapped in Brazil, March) seasons, with mild mean annual temperatures where endemic and threatened species occur (Develey & (18–19°C) and low (0°C or less) temperatures mainly at Goerck 2009, BirdLife International 2014). Nevertheless, higher elevations (Dutra et al. 2002). The Köppen-Gei ger several problems have been reported regarding human climatological classifi cation defi nes this area as Cwb interference in areas devoted to conservation, for example, (humid temperate climate with dry winters and temperate exploration of land use in surroundings, fragmentation, summers, similar to tropical climate of altitude) (Alvares et al. 2013) and the annual average rainfall is above 1500 wildfi res and ineff ective surveillance (Lima et al. 2005, Rylands & Brandon 2005). mm. Records for bird collisions with aircraft, power lines In the area 372 bird species had been recorded, and vehicles have been increasing in Brazil, but there including 13 threatened species, 75 migrants, 74 Atlantic remains much to be understood about this phenomenon Forest endemics, four Cerrado endemics and four species restricted to mountain-tops of southeastern Brazil (Nascimento et al. 2005, Laurance et al. 2009, Rosa & Bager 2012). Only a few studies have focused on bird (Chesser 1994, Vasconcelos 2013). Serra do Caraça has mortality due to collisions with man-made structures in one of the richest avifaunas of eastern Brazil, it is an Brazil (ACS 2006, Carrano 2006, Muhlenberg College important area for bird conservation on both regional and 2009, Santos et al. 2011, Soares et al. 2011, Stolk et global scales (Vasconcelos & Melo-Júnior 2001, Bencke et al. 2006, Develey & Goerck 2009). Th e area is located al. 2015), making it difficult to make comparisons and determine influential factors. This is particularly true in an IBA (BR145; BirdLife International 2009, 2012, given the great bird diversity of Brazil and the large size Develey & Goerck 2009), an Endemic Bird Area (EBA of the country, thereby confounding attempts to develop 073; Stattersfield et al. 1998) and a Biosphere Reserve preventive measures or findin g solutions. (UNESCO 2005). In this paper, we report on bird collisions with windows in a Brazilian protected area and IBA, considering Data collection characteristics such as forest dependence, wing type, threaten status, endemism and migratory habits of each Th e RPPNSC is locally well known for its historical man- species. We also tested for a seasonal relationship between made architecture. One of the buildings is the Caraça Museum (Fig. 1), which is 70 m nearly from the forested seasons (dry and rainy) and the number of dead birds. vegetation and has sides that comprised large, reflective tempered glass windows (Fig. 2). On those windows METHODS (408.5 m ) occur bird collisions under investigation in the present study. Study area Dead birds were collected daily, but stored in freezer by monthly lots, during 2010 to 2013, with Th e Reserva Particular do Patrimônio Natural Santuário do the assistance of the environmental team of RPPNSC. o o Caraça a (hereafter RPPNSC - 20 05'51"S; 43 29'18"W; Additional casual non-systematic records were carried out elevation 1290 m a.s.l.), located in the municipalities during 2000–2009 and 2014–2015. Specimens found of Catas Altas and Santa Bárbara, state of Minas Gerais, dead were placed in individual plastic bags with a label Revista Brasileira de Ornitologia 25(2): 2017 Bird mortality due to collisions in glass panes Santos et al. R R R R R R R :  :  :  :  : R R Figure 1. Location map ( ( (A A A) and aerial image of the Reserva Particular do Patrimônio Natural Santuário do Caraça, showing the architectural complex (B). The dark grey box is the Caraça Museum with sides ( ( (A–D) comprised of windows. P P Figure 2. Architectural sketch of Caraça Museum showing the details of the building and the width, height and depth of its sides. Percentage and area (in m ) of glass (grey areas) on each side of the Caraça Museum: ( ( (A A A)  31% (110); (B)  90% (151.5); (C) 34.9% (124.2); (D)  13.6% (22.8). Revista Brasileira de Ornitologia 25(2): 2017 Bird mortality due to collisions in glass panes Santos et al. dead from collision between the two seasons (dry and containing basic collection data and frozen. Specimens rainy) we used the Shapiro-Wilk test for normality were deposited (mostly as study skins and/or skeletons) in and, subsequently, t t t-test for two independent samples the following collections: Museu de Ciências Naturais da (parametric). The F F F-test was used to compare sample Pontifícia Universidade Católica de Minas Gerais (MCNA), distributions of the two seasons. We analyzed the Department of Zoology of the Universidade Federal de seasonality only for specimens for which the month of Minas Gerais (DZUFMG) and Museu de Zoologia da their collision was known. A rate per day (the number of Universidade de São Paulo (MZUSP). We identified all collided birds by the total of days in each season) was used individuals to species level following nomenclature in for comparison between the systematic sampling periods. Piacentini et al. (2015). Using monthly rainfall (in mm) at RPPNSC during 2010–2013, we assessed diff erences in rainfall for each Data analysis season using factorial ANOVA. To evaluate rainfall as a factor of bird mortality, we performed a Pearson product We classified the s pecimens qualitatively and moment correlation between average monthly rainfall and quantitatively for attributes from the literature: I) Forest number of individuals found dead from collision. dependence (Silva 1995, Parker-III et al. 1996): 1) independent (species that occur in open vegetation), 2) Statistical analyses were conducted in R Software (R Core Team 2017;  = 0.05) and used all birds found dead semi-dependent (species that occur in open vegetation as a result of colliding with the windows of the Caraça and forest), and 3) dependent (species found mainly in forest habitats); II) Wing types (Scott & McFarland Museum. Plotrix package v. 3.6-1 (Lemon et alll. 2015) was used for producing the radial graph. 2010): 1) elliptical, 2) game bird, 3) high-aspect ratio, 4) high-speed, and 5) slotted high-lift; III) Th reat status: 1) global (IUCN 2015), 2) national (MMA 2014a, b), and RESULTS 3) state (COPAM 2010); IV) Endemism: 1) Cerrado (Silva 1995), 2) Atlantic Forest (Brooks et al. 1999) and 3) mountaintops of eastern Brazil (Vasconcelos 2008); A total of 168 specimens of 57 species (Appendix I) were found dead presumably due to collisions with glass panes and V) Migration: austral migrants (sensu Chesser 1994). of the Caraça Museum. Th e mortality rates for the period To test for significant differences in the proportions of systematic sampling (102 individuals in 2010–2013) were of  2.12 deaths/month and 25.50 deaths/year. of collided birds among categories of forest dependence and wing types, we use separate Chi-Square tests with no Th e orders most aff ected were Passeriformes diff erence among categories as the expected proportion. (102 individuals) and Columbiformes (44) (Table 1). Regarding families, the most affected were Columbidae We also performed Partition Likelihood Ratio Chi- Square to evaluate relationships between categories of (44 individuals), Thrau pidae (35), Trochilidae (16) and both of these characteristics. Hirundinidae (15), whereas the most affected genera To test for diff erences in the number of birds were Turdus s (13) and Tangara a (11). The most commonly Table 1. Orders of birds dead due to collisions with windows of the Caraça Museum, Minas Gerais state, Brazil, and the number of individuals for each category of forest dependence and wing type. Dependent 2 1 41 0 9 0 0 44 97 Semi-dependent 0 0 3 1 6 1 1 27 39 Independent 0 0 0 0 1 0 0 31 32 Elliptical 0 1 44 0 0 1 0 87 133 High-speed 0 0 0 1 16 0 0 15 32 Slotted 0 0 0 0 0 0 1 0 1 Game Bird 2 0 0 0 0 0 0 0 2 Total 2 1 44 1 16 1 1 102 168 Revista Brasileira de Ornitologia 25(2): 2017 Galiiformes Accipritiformes Columbiformes Psitaciformes Apodiformes Coraciiformes Piciformes Passeriformes Total Bird mortality due to collisions in glass panes Santos et al. encountered species were the Plumbeous Pigeon (Patagioenas plumbea) (35 individuals) and the Blue-and- white Swallow (Pygochelidon cyanoleuca) (13). We found greater mortality for forest dependent (97 individuals; 57.8%) and semi-dependent (39; 23.2%) species than independent species (32; 19.0%). Forest dependence had the greatest influence on bird mortalit y ( = 46.46; P < 0.0001). Among wing types, species classified as having elliptical wings were the most affected (133 individuals; 79.2%), followed by high-speed (32; 19%), game bird (2; 1.2%) and slotted high-lift (1; 0.6%) wings. Elliptical wings diff ered signifi cantly from the other categories of wing types ( = 277.67; P < 0.0001). The interaction between the natural history characteristics of forest dependence and wing type had a significant general value (Table 2). A significant diff erence was found for partition one ( = 24.11; 2×3 tables P = 0.0001), demonstrating that individuals classified as Fi Figure 3 3. R Radi diall graph h of f th he average numb ber of f i indi divid idualls forest dependent with elliptical wings are more frequently found dead in each month of the two study seasons (polygon; light grey: dry season; dark grey: rainy season; grid scale: 0–14). aff ected by collisions. Data points (in black) and respective numbers reveal the average In relation to threaten status, only two species monthly rainfall (mm) for 2010–2013 in RPPN Santuário do were considered globally “Near Th reatened”: the Caraça a (grid scale: 0–700). Hyacinth Visorbearer Augastes scutatus s (1 individual) and the Swallow-tailed Cotinga Phibalura flavirostris s (2 individuals); the latter is also considered “Vulnerable” DISCUSSION in the state of Minas Gerais. All other specimens were classifi ed as “Least Concern” species at the global, national Sixteen percent of the total number of bird species known and/or state levels. to occur in RPPNSC was aff ected by collisions with the Endemic species were represented by 38 specimens of studied structure. However, it is important to stress that, the Atlantic Rain Forest and one (Hyacinth Visorbearer) even with the helpful assistance of the environmental from the mountains of eastern Brazil. Twenty-seven individuals of 10 species of austral migrants were found team of the reserve, it is possible that several dead specimens were overlooked. Specimens may have been dead by collisions throughout our study. missed due to their rapid decomposition due to natural No significant seasonal mortality pattern was found factors such as weather, sunlight, rain, necrophagous between the rainy (44 individuals; rate [collided birds/ animals (invertebrates such as ants, fl ies, beetles) and rainy days] = 16.56) and dry (54; rate [collided birds/ dry days] = 13.55) seasons (t t = 0.96; P P = 0.362; F F = 1.01; other biological agents (bacterial digestion) (Crawford 1971, Balcomb 1986, Pain 1991, Wobeser & Wobeser P P = 0.99) (Fig. 3). The significant difference in monthly 1992). Scavengers and opportunist vertebrate predators rainfall between the seasons (F F F(seasons) = 37.44; P < also can remove small bird carcasses within a matter of a 0.0001) was not correlated with bird mortality. Table 2. Number of individuals dead due to collisions with windows of the Caraça Museum, Minas Gerais state, Brazil, classifi ed by category of interaction between forest dependence and wing type. Categories Dependent Semi-dependent Independent Elliptical 86 31 16 High-speed 9 7 16 Game bird 2 0 0 Slotted high-lift 0 1 0 Chi-square value 30.295 Significance level P P < 0.0001 Revista Brasileira de Ornitologia 25(2): 2017 Bird mortality due to collisions in glass panes Santos et al. few minutes after death and it is also believed that many Columbiformes, can be related with the susceptible when collisions may not result in immediate death, which may they cross open environments and other characteristics, imply that most of the studies on bird mortality due such as photophobia and forest proximity. to human factors are underestimates (Klem-Jr. 1990a, Sporer et al. (2013) noted that high-speed and Morris 2002, Antworth et al. 2005, Kummer et al. 2016). elliptical-winged birds frequently collide with power Forest dependent birds were most frequently aff ected lines. High-speed birds were represented in our sample by collisions in RPPNSC. We interpret this as the Caraça by some species of Trochilidae and Hirundinidae, which Museum building disrupts a natural corridor formed not only possess fast flight, but also can remain in by the surrounding vegetation, and forest birds fail to flight for a greater period of time (Scott & McFarland recognize this obstacle as a change of habitat. In contrast, 2010). Jenkins et al. (2010) pointed out that high speed the lower number of forest independent species can be affects the reaction time of bir ds to avoid collisions with attributed to their ability to recognize edges in open areas, anthropic structures. Game birds, which generally have since these species should have a better perception of slotted and high-aspect wing types, were not abundant in obstacles, and thus be more able to avoid them. our sample, and exhibit other fli ght performances such as In general, forest dependent species react more soaring, lift and difficult take-offs. negatively to environmental changes than forest The frequency of collisions with the large windows independent species. For example, the presence of forests of the Caraça Museum can be evaluated in the context next to roads increased roadkill of forest species (Marini of the surrounding landscape and thus the reflections o f 2001, Ramos et al. 2011). Although it is known that the vegetation in the windows (Ogden 1996, Gelb & forest birds avoid crossing large open areas (Grubb-Jr. & Delacretaz 2009, Klem-Jr. 2009). Th e Caraça Museum is Doherty-Jr. 1999, Develey & Stouff er 2001), these species adjacent to a large forested area, but is situated in an open perform frequent movements in their environments space inside the architectural complex. Sensory analyses and may cross-forest fragments, especially those species have determined that birds perceive such reflections adapted to patchy environments (Marini 2001, Yabe et as an extension of the physical environment, and their al. 2010). visual system is not exclusively dedicated to perceiving The hi gh incidence of collisions by native pigeons fi xed obstacles, such as human structures, thus eventually (Columbidae), especially the Plumbeous Pigeon, leading to collisions with windows (Martin & Shaw signifi cantly infl uenced the interpretation of our analysis. 2010, Martin 2011). Perhaps the abundance of this species in RPPNSC, and Our data did not show any seasonal diff erence in bird the patterns of its biological activities, such as feeding, mortality between dry and rainy seasons. Th e RPPNSC dispersal and reproduction are responsible for the experiences high variation in monthly rainfall, but slight high collision rate of this species. In conjunction, the oscillations in other abiotic factors such as temperature abundance and differential use of s pecific habitats b y and wind speed and direction, as has been reported bird populations is also of fundamental importance to previously (Moreira & Pereira 2013). A relationship predicting collisions (De Lucas et al. 2008, Marques et between bird collisions with artifi cial structures and al. 2014). Other studies also report a high incidence of seasonal patterns can be more important in regions where accidents with Columbidae species, including birdstrikes climate conditions exhibit larger variations, but is also on aircrafts and windows collisions (Dolbeer 2006, related to routes and additional types of migrant species Kitowski 2011, Ocampo-Peñuela et al. 2016). (e.g. Klem-Jr. 1989, Borden et alll. 2010). Diff erent wing types are associated with diff erent Other weather and meteorological factors, such as fli ght performances (Warham 1977, Copete 1999). In daily temperature, air humidity, sunlight, clouds and the case of power lines, fl ight behavior is one of the most mist, change the perception of, and interaction with, important biological features for bird collisions (Bevanger the physical environmental by birds (e.g. Bevanger 1994, Janss 2000). Th e prominent number of collisions 1994, Drewitt & Langston 2008, Martin 2011). In the by birds with elliptical wings in the present study indicates Neotropical region, the infl uence of these conditions on that birds with this characteristic have a greater tendency bird collisions is still unknown, and there certainly are for collisions. Scott and McFarland (2010) explain that other environmental factors shaping this interaction, birds with elliptical wings have quick bursts of speed and such as changes in the composition of food resources or are most adept at navigating densely vegetated habitats. patterns of other biological activities. Further exploration This fact contextualizes the hi gh representation of this of seasonal patterns of birds may help to uncover category in our sample, especially due to the proximity fundamental answers about bird collisions, and provide of vegetation to the Caraça Museum. Further, the strong important information for strategies to mitigate this association of elliptical wings and forest dependent birds, problem (Borden et alll. 2010). which the most represented orders were Passeriformes and It is important to stress that all bird species are not Revista Brasileira de Ornitologia 25(2): 2017 Bird mortality due to collisions in glass panes Santos et al. of scavenging on estimates of roadkilled vertebrates. Southeastern equally susceptible to mortality by collisions (Bevanger Naturalist t 4: 647–656. 1994, Drewitt & Langston 2008, Loss et al. 2014). APLIC (Avian Power Line Interaction Committee). 2012. Reducing Borden et al. (2010) mention that bird collisions are a avian collisions with power lines: the state of the art in 2012. complex question and there are no simple relationships Washington: Edison Electric Institute and Avian Power Line that explain it in its entirety. Furthermore, species Interaction Committee. Avery M.L. 1979. 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APPENDIX I List of species found dead due to collisions with the Caraça Museum (RPPN Santuário do Caraça) and their respective data, as follow: Forest dependence: D - Dependent; S - Semi-dependent and; I - Independent; Wing type: E - Elliptical; HS - High-Speed; ST - Slotted; GB - Game Bird; Conservation Status: LC - Least Concern; NT - Near G N S Th reatened; Globally Level; National Level; State Level; Seasonality: month of collision (number of individuals AF MT M that collided); Atlantic Rain Forest Endemism; Mountaintops of Southeastern Brazil Endemism; Migratory species. Taxon Cracidae Rafi nesque, 1815 Dusky-legged Guan G, N, S 2 D GB LC 2 (1), 4 (1) Penelope obscura Temminck, 1815 Accipitridae Vigors, 1824 Bicolored Hawk G, N, S 1 D E LC - Accipiter bicolor (Vieillot, 1817) Columbidae Leach, 1820 Blue Ground-Dove G, N, S 1 S E LC 11 (1) Claravis pretiosa (Ferrari-Perez, 1886) Plumbeous Pigeon 1 (4), 2 (2), 4 (2), 5 (1), G, N, S 35 D E LC Patagioenas plumbea (Vieillot, 1818) 6 (1), 9 (1), 12 (2) White-tipped Dove G, N, S 2 S E LC 1 (1) Leptotila verreauxi Bonaparte, 1855 Gray-fronted Dove G, N, S 4 D E LC 4 (2) Leptotila rufaxilla (Richard & Bernard, 1792) Ruddy Quail-Dove G, N, S 2 D E LC 6 (1), 9 (1) Geotrygon montana (Linnaeus, 1758) Psittacidae Rafines que, 1815 White-eyed Parakeet G, N, S 1 S HS LC - Psittacara leucophthalmus s (Statius Muller, 1776) Trochilidae Vigors, 1825 Planalto Hermit G, N, S 1 S HS LC - Phaethornis pretrei i (Lesson & Delattre, 1839) AF Scale-throated Hermit G, N, S 1 D HS LC 7 (1) Phaethornis eurynome (Lesson, 1832) White-vented Violetear G, N, S 1 S HS LC 4 (1) Colibri serrirostris s (Vieillot, 1816) Glittering-bellied Emerald G, N, S 3 S HS LC 3 (1) Chlorostilbon lucidus s (Shaw, 1812) AF Violet-capped Woodnymph G, N, S 1 D HS LC 7 (1) Thalurania glaucopis (Gmelin, 1788) Versicolored Emerald G, N, S 1 D HS LC 10 (1) Amazilia versicolor (Vieillot, 1818) Sapphire-spangled Emerald G, N, S 3 D HS LC 4 (1), 6 (1), 7 (1) Amazilia lactea (Lesson, 1832) AF Brazilian Ruby G, N, S 3 D HS LC 10 (1) Heliodoxa rubricauda (Boddaert, 1783) MT Hyacinth Visorbearer G N, S 1 I HS NT ; LC 4 (1) Augastes scutatus (Temminck, 1824) Amethyst Woodstar G, N, S 1 S HS LC - Calliphlox amethystina (Boddaert, 1783) Revista Brasileira de Ornitologia 25(2): 2017 Number of individual Forest dependence Wing type Conservation status Seasonality Bird mortality due to collisions in glass panes Santos et al. Taxon Alcedinidae Rafinesque, 1815 Green Kingfisher G, N, S 1 S E LC 1 (1) Chloroceryle americana (Gmelin, 1788) Ramphastidae Vigors, 1825 Toco Toucan G, N, S 1 S ST LC - Ramphastos toco Statius Muller, 1776 Thamnophilidae Swainson, 182 4 AF Large-tailed Antshrike G, N, S 1 D E LC 7 (1) Mackenziaena leachii (Such, 1825) Furnariidae Gray, 1840 Rufous Hornero G, N, S 1 I E LC - Furnarius rufus s (Gmelin, 1788) AF Pallid Spinetail G, N, S 2 D E LC 2 (1), 8 (1) Cranioleuca pallida (Wied, 1831) Pipridae Rafines que, 1815 AF Serra do Mar Tyrant-Manakin G, N, S 1 D E LC 9 (1) Neopelma chrysolophum Pinto, 1944 White-bearded Manakin G, N, S 1 D E LC 5 (1) Manacus manacus (Linnaeus, 1766) AF Pin-tailed Manakin G, N, S 2 D E LC 9 (1) Ilicura militaris (Shaw & Nodder, 1809) AF Swallow-tailed Manakin G, N, S 4 D E LC 4 (1), 5 (1), 6 (1) Chiroxiphia caudata (Shaw & Nodder, 1793) Tityridae Gray, 1840 White-winged Becard G, N, S 1 S E LC 9 (1) Pachyramphus polychopterus (Vieillot, 1818) Cotingidae Bonaparte, 1849 M G N Swallow-tailed Cotinga NT ; LC ; 2 D E 11 (1) Phibalura flavirostri s Vieillot, 1816 VU Rhynchocyclidae Berlepsch, 1907 AF Gray-hooded Flycatcher G, N, S 5 D E LC 6 (2), 11 (1) Mionectes rufi ventris Cabanis, 1846 AF Hangnest Tody-Tyrant G, N, S 2 S E LC 6 (2) Hemitriccus nidipendulus (Wied, 1831) Tyrannidae Vigors, 1825 Great Kiskadee G, N, S 2 I E LC - Pitangus sulphuratus (Linnaeus, 1766) AF Velvety Black-Tyrant G, N, S 6 S E LC 5 (1), 6 (2) Knipolegus nigerrimus (Vieillot, 1818) Hirundinidae Rafinesque, 181 5 Blue-and-white Swallow G, N, S 13 I HS LC 1 (3), 10 (1), 12 (4) Pygochelidon cyanoleuca (Vieillot, 1817) Southern Rough-winged Swallow G, N, S 2 I HS LC - Stelgidopteryx rufi collis (Vieillot, 1817) Turdidae Rafinesque, 181 5 Yellow-legged Thrush G, N, S 3 D E LC 4 (1) Turdus flavipes Vieillot, 1818 Pale-breasted Thrus h G, N, S 1 S E LC - Turdus leucomelas Vieillot, 1818 Rufous-bellied Thrus h G, N, S 2 I E LC 12 (1) Turdus rufi ventris Vieillot, 1818 Revista Brasileira de Ornitologia 25(2): 2017 Number of individual Forest dependence Wing type Conservation status Seasonality Bird mortality due to collisions in glass panes Santos et al. Taxon Creamy-bellied Thrush G, N, S 2 S E LC 10 (2) Turdus amaurochalinus Cabanis, 1850 White-necked Thrus h G, N, S 5 D E LC 7 (1), 8 (1), 12 (1) Turdus albicollis Vieillot, 1818 Passerellidae Cabanis & Heine, 1850 Rufous-collared Sparrow G, N, S 1 I E LC 1 (1) Zonotrichia capensis s (Statius Muller, 1776) Icteridae Vigors, 1825 Red-rumped Cacique G, N, S 2 S E LC 2 (1), 11 (1) Cacicus haemorrhous (Linnaeus, 1766) Shiny Cowbird G, N, S 1 I E LC - Molothrus bonariensis s (Gmelin, 1789) Th raupidae Cabanis, 1847 Cinnamon Tanager G, N, S 1 I E LC 11 (1) Schistochlamys rufi capillus (Vieillot, 1817) Sayaca Tanager 2 (1), 8 (1), 9 (1), 10 G, N, S 6 S E LC Tangara sayaca (Linnaeus, 1766) (1) Palm Tanager G, N, S 1 S E LC 8 (1) Tangara palmarum (Wied, 1821) AF Golden-chevroned Tanager G, N, S 2 D E LC 2 (1) Tangara ornata (Sparrman, 1789) Burnished-buff Tanager G, N, S 2 I E LC - Tangara cayana (Linnaeus, 1766) Saff ron Finch G, N, S 3 I E LC - Sicalis flaveolaa (Linnaeus, 1766) AF Uniform Finch G, N, S 4 D E LC 4 (1), 7 (1), 12 (1) Haplospiza unicolor Cabanis, 1851 AF Black-goggled Tanager G, N, S 1 D E LC 8 (1) Trichothraupis melanops (Vieillot, 1818) AF Ruby-crowned Tanager G, N, S 4 D E LC 4 (1), 8 (1), 9 (1) Tachyphonus coronatus (Vieillot, 1822) Swallow Tanager G, N, S 1 D E LC 4 (1) Tersina viridis (Illiger, 1811) Blue Dacnis G, N, S 5 S E LC 7 (1) Dacnis cayana a (Linnaeus, 1766) Sporophila a sp. 2 I E - 1 (1) Yellow-bellied Seedeater G, N, S 1 I E LC 7 (1) Sporophila nigricollis (Vieillot, 1823) Green-winged Saltator G, N, S 1 S E LC - Saltator similis s d'Orbigny & Lafresnaye, 1837 Fringillidae Leach, 1820 Blue-naped Chlorophonia G, N, S 6 D E LC 3 (1), 6 (1), 7 (1) Chloroppy honia cyanea (Thunber g g, 1822) Revista Brasileira de Ornitologia 25(2): 2017 Number of individual Forest dependence Wing type Conservation status Seasonality

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Ornithology ResearchSpringer Journals

Published: Jun 1, 2017

Keywords: bird collisions; mortality; natural history; RPPN Santuário do Caraça; seasonality

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