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Influence of urbanization on the distribution and defense strategies of the Burrowing Owl Athene cunicularia in the city of Uberlândia, southeastern Brazil

Influence of urbanization on the distribution and defense strategies of the Burrowing Owl Athene... Revista Brasileira de Ornitologia 26(1): 1–8. ARTICLE March 2018 Influence of urbanization on the distribution and defense strategies of the Burrowing Owl Athene cunicularia in the city of Uberlândia, southeastern Brazil 1,2,3 2 Felipe Fina Franco & Oswaldo Marçal-Junior Graduate Program in Ecology and Conservation of Natural Resources, Institute of Biology, Federal University of Uberlândia, Campus Umuarama, Rua Ceará s/n, Bloco 2D, sala 34, Uberlândia, MG, 38400-902, Brazil. Laboratory of Ornithology and Bioacustics, Federal University of Uberlândia, Campus Umuarama, Rua Ceará s/n, Bloco 2D, sala 34, Uberlândia, MG, 38400-902, Brazil. Corresponding author: felipefinafranco@hotmail.com Received on 19 September 2017. Accepted on 19 January 2018. ABSTRACT: Urbanization causes drastic changes in habitat and species behavior. In birds, these changes influenced t he extinction of some species. The Burrowing Owl Athene cunicularia (Molina, 1782) (Aves: Strigiformes) has achieved some success in its adaptive process in anthropic environments. The main objective of this study was to measure distribution of this species in urban areas. The specific o bjectives were to quantify and compare the occurrence of this owl and its satellite burrows among urban biotopes; evaluate the importance of satellite burrows as a defense strategy and compare the depth of burrows in different biotopes. Field activities were carried out from August 2015 to November 2016. Sixty areas were sampled in different urban regions. The species was present in 29 of the 60 sites investigated, totaling 112 individuals, 88 adults, 14 young and 10 chicks; 98 burrows were recorded, from which 22 were refuges, seven nests and 67 satellite burrows. Residential and Urban Green Area biotopes had the highest number of individuals and burrows with a significant difference relative to the Commer cial/Industrial biotope. A greater number of individuals were found in areas with a high number of burrows showing a positive linear relationship between these variables. The burrows were deepest, on average, in Urban Green Area biotopes. We conclude that the species has a wide distribution in the city with significantly high numbers in the Residential biotope. This same tendency is verified for the distribution of burrows. In areas with a large number of individuals, the same was observed for the number of satellite burrows. Deeper burrows in the Urban Green Areas are perhaps due to the greater transit of people, one of the main features of this biotope and one of the major threats to the Burrowing Owls. KEY-WORDS: biotope, habitat, occurrence, satellite burrows, survival. INTRODUCTION having an important role in the food chain (Millennium Ecosystem Assessment 2005). In addition, they perform Urbanization can be defined as a process of anthropic functions like pollination and dispersal of fruits and seeds occupation that gradually transforms natural (Silva & Nakano 2008). environments and includes the presence of relatively Some of these birds live in urban environments, permanent human populations on the site (Marzluff such as Athene cunicularia (Molina, 1782), that is widely distributed throughout the Americas, from Canada et al. 2001). On a global scale, anthropic pressures have influenced t he structure and behavior of faunal to southern Argentina (Poulin et al. 2005, 2011). populations and communities, and also of ecosystems Burrowing Owls have preference for open habitats, in remnants of natural areas (Bradshaw & Holzapfel foraging and breeding in short, low-density vegetation 2006, Delibes et al. 2011). Human presence can lead to and mainly grasslands (Rebolo-Ifrán et al. 2017). These owls are common in Brazil and known for being urban population decline, persistence, or even the expansion of bird distributions (Sih et al. 2011). Furthermore, the dwellers, showing behavioral adjustments to anthropic- disturbances caused by anthropic actions seem to be altered environments (although they are commonly causing changes in the distribution and behavior of birds observed in natural areas) (Sick 1997, Motta-Junior and might also be leading many species to extinction & Alho 2000). Some populations are able to exploit human-made habitats with a preference for urban over (Silva & Nakano 2008). Many birds have adapted to the anthropic rural areas (natural grasslands and low-intensive agro- environment and their presence is important for pest pastoral lands) (Rebolo-Ifrán et al. 2017). Main causes control, such as predation of rats and insects, besides of mortality include collisions with vehicles and nest Influence of urbanization on Athene cunicularia Franco & Marçal-Junior destruction (Silva 2002). The behavioral responses of METHODS Burrowing Owls to threats can be easily recognized, such as the use of deep burrows, use of satellite burrows, flying Study area and data collection away in the presence of potential predators, making alarm calls, adopting threat postures and some type of attacks The municipality of U berlândia has about 669,000 (Coulombe 1971, Thomsen 1971, Fisher et al. 2004). habitants (IBGE 2016), with a total area of 4040 km in Burrowing Owls are present in many parts of the the state of Minas Gerais (MG), southeastern Brazil, from world and are considered one of the main predator which 219 km are urban. In areas surrounding the city, species of rodents in urban areas (Martins & Eagler 1990, the native vegetation was reduced to remnants of less than Sick 1997, Motta-Junior & Alho 2000). However, the 15% of the original cover, with evident reduction of the behavior of the species is affected by urbanization and it local fauna (Brito & Prudente 2005). is reported that the increase in vehicular traffic around We visited areas with a potential occurrence of the the nest produces an increase in the couple's waking species, typically with short grasses and wide spaces of time (Plumpton & Lutz 1993). Similarly, populations open areas (Coulombe 1971, Plumpton & Lutz 1993, of Burrowing Owls are under heavy pressure from Marks et al. 1999). Field activities were carried out from domestic animals, such as dogs and cats (Dechant et al. August 2015 to November 2016, with monthly data 2003, Rosenberg & Haley 2004, Moulton et al. 2006). collections along the day (from 7:00 h to 18:00 h) with These threats determine behavioral responses that include small interruptions, not every day of the month, and subterranean retreat, deeper burrows, the use of satellite totaling 2000 h of observation. burrows, the issuance of alarm calls, and dive-in-flight Sixty sites (with areas of about 33 m each) were attacks (Coulombe 1971, Thomsen 1971, Fisher et al. sampled in different parts of the city, 20 per urban biotope, 2004). It has also been described the use of mammalian and visited monthly. The minimum distance between sites manure, placed near the entrance of the burrow, to avoid was 200 m, in order to guarantee the independence of potential predators with bad odor (Martin 1973). the samples and considering the territorial behavior of the Burrows are the essential component of Burrowing studied species (Gaston 2003). These sites were selected Owl habitat: both natural and artificial burrows provide according to the potential occurrence of the Burrowing protection, shelter, and nests (Henny & Blus 1981). Owls with the help of satellite images obtained from the Burrowing Owls typically use burrows made by fossorial Google image bank of the city of Uberlândia (Google mammals, but also may use man-made structures, such Earth 5.1 2009) and also by direct field o bservations. All as cement culverts; cement, asphalt, or wood debris sites were georeferenced by taken a point in the middle piles; or openings beneath cement or asphalt pavement. using a Global Positioning System (GPS) and a map of Burrowing Owls exhibit high site fidelity, reusing burrows the city was made with these GPS points in the software year after year (Rich 1984, Feeney 1992). Once young QGIS 2.18.2 (Fig. 1). individuals learn to fly, the family group often moves Biotope refers to a certain living space distinct from from one burrow to another (Thomsen 1971). the others, endowed with environmental conditions Declines in populations of this species in North suitable for specific organisms (Sukopp & Weiler America called the attention of environmentalists 1988). The selected sites were classified a ccording to (Holroyd et al. 2001, Skeel et al. 2001, Warnock & Skeel the European Method for Mapping Biotopes: Urban 2004, Conway & Pardieck 2006) and, in Florida, the Green Areas, Residential and Commercial/Industrial Burrowing Owl had its status updated to threatened in (Sukopp & Weiler 1988, Weber & Bedê 1998). Urban the state red lists (Florida Fish and Wildlife Conservation Green Areas include urban parks, squares, sports Commission 2017). The aim of the present study was centers, theaters, universities, schools and airports, to determine the distribution and the abundance of the all places in which there is a high flow of people and a Burrowing Owl in urban areas of the city of Uberlândia, medium level of urbanization. The residential biotope is southeastern Brazil, by (1) evaluating the occurrence and characterized by the presence of houses, condominiums abundance of the species among different urban biotopes; and residential buildings, with less evident levels of (2) determining the occurrence and distribution of pollution and environmental disturbances; in addition, burrows (satellites, nests or refuges) per urban biotopes; this biotope has a lower flow of humans and ve hicles (3) evaluating different defense mechanisms, such as the (but with constant presence of domestic animals). The importance of satellite burrows, the relationship between Commercial/Industrial biotope includes open areas with the number of individuals and burrows; and the depth of short grasses, near places with intense commerce, such as the burrows in different biotopes, which are fundamental malls, industries or construction sites, with intense traffic aspects for conservation of the studied species in modified of vehicles and high level of urbanization. environments. Three visits were conducted to each site, totaling 180 Revista Brasileira de Ornitologia 26(1): 2018 Influence of urbanization on Athene cunicularia Franco & Marçal-Junior Figure 1. A map of the distribution of the sampled points for the Burrowing Owl occurrence, according to the investigated biotopes (Urban Green Area, Residential or Commercial/Industrial) in the urban area of Uberlândia (MG), Brazil. visits (60 visits in each biotope investigated). The relative biotopes we used the ANOVA One-Factor test. Tukey's abundance was calculated by counting individuals of test was used to determine which factor levels (urban the target species per site and the same was done for the biotope) differed from each other (Zar 2010). Another burrows. Individuals were classified a ccording to gender ANOVA test was used to evaluate the differences in (only adults) (Zarn 1974) and age group (adults, chicks burrow depth by biotope. and juveniles) (Appendix I). Burrows were classified as To evaluate the correlation between number of main or satellite. Main burrows were subdivided by nests individuals and burrows we performed a simple linear (in which chicks or eggs were present) and refuges (in regression. Values were square root transformed for which only adults were present). Satellite burrows were normality adjustment (Zar 2010). All statistical analyzes represented by non-inhabited burrows near the main were performed using the Systat 10.2 software, with a ones, and are used as a defense mechanism against threats, significance level of  = 0.05 (Zar 2010) and graphs were in which individuals rotate between burrows in order to built using Illustrator 21.1.0. confuse predators (Henny & Blus 1981, Desmond & Savidge 1999). Some burrows were lost due to human action. RESULTS To measure the depth of the burrows we used a digital measuring tape (Bosch GLM30) 5 m long. Only Distribution, occurrence and abundance burrows that we could reach without causing stress (absence of individuals) or nests without the presence of The species was found in 29 out of the 60 sampled sites chicks, were measured. (48%). In total, 98 burrows were registered, with a mean of 3.14 burrows per point, with 29 main burrows (22 Data analysis refuges and seven nests) and 69 satellite burrows. We recorded 112 individuals (Table 1). Homogeneity tests of variances and normality of the sampled data were performed using a Lilliefors test and by Distribution and occurrence by biotopes evaluating the data distribution in scatter plots. Sample data transformations (three times in the Variance Analysis, Residential biotope points showed the highest number of individuals (n = 55) followed by Green Urban Area in addition to the Linear Regression) were performed by square rooting values, which were necessary due to the points (n = 47) and Commercial/Industrial Area points (n non-normality distribution of the sampling data (Zar = 10). The largest number of individuals found in a single 2010). To determine the differences in Burrowing Owl point was recorded in a Residential biotope (n = 8). A abundance and number of burrows according to urban mean of three individuals per point were recorded in the Revista Brasileira de Ornitologia 26(1): 2018 Influence of urbanization on Athene cunicularia Franco & Marçal-Junior Table 1. Number of individuals of Burrowing Owl, by age group (adults, juveniles and chicks) and gender (male and female) in the biotopes investigated in the urban area of Uberlândia (MG), Brazil. Adults Biotopes Chicks Juveniles Total Male Female Residential 21 22 9 3 55 Green Urban Area 18 18 4 7 47 Commercial/Industrial 36 1 0 10 TOTAL 42 46 14 10 112 Residential biotope, two in Green Urban Area and 0.5 in Commercial/Industrial (F = 4.2, P = 0.020, Fig. 2A), (2,57) with a significant difference between the Residential and Commercial/Industrial biotopes (P < 0.016). Distribution and occurrence of burrows by biotopes We found 51 burrows in the Residential biotope, 39 in Green Urban Area and 8 in Commercial/Industrial (F (2,57) = 3.19, P = 0.048, Fig. 2B), with a significant difference between Residential and Commercial/Industrial (Tukey's test; P < 0.040). Relationship between satellite burrows and number of individuals In general, large numbers of satellite burrows were found in points with large number of individuals, with a positive Figure 2. (A) Mean of individuals of Burrowing Owl per point linear relationship between the two variables (F = distributed according to the biotopes (G.U.A = Green Urban (1,58) 428.89, P < 0.001, R > 0.88) (Fig. 3) (Table 2). Area; COM/IND = Commercial/Industrial) in Uberlândia (MG), Brazil; (B) Mean number of burrows per point, showing a relationship between burrows (refuges, satellites and nests) Depths of burrows in the urban biotopes and biotopes (G.U.A = Green Urban Area; COM/IND = Commercial/Industrial) of the Burrowing Owl in Uberlândia Thirty-four depths of burrows were measured. The (MG), Brazil. Confidence intervals were considered for P < highest mean was observed in the Green Urban Area 0.05. biotope, reaching a maximum depth of 3.5 m. There was a significant difference between the three biotopes (F (2,17) different human-altered habitats (Sih et al. 2011, Sol et al. = 4.05, P < 0.030, Fig. 4), with the greatest depths in the 2013, Rebolo-Ifrán et al. 2017). On the other hand, some Green Urban Area (P = 0.049). studies indicate that urbanization leads to the population decline of Burrowing Owls (Millsap & Bear 2000, Jones DISCUSSION & Bock 2002, Chipman et al. 2008). This decline is attributed to the loss of habitat to cultivation and other The results obtained corroborated other studies (Haug et land use activities, predation by domestic animals and al. 1993, Holmes 1998, Chipman et al. 2008, Berardelli human persecution, amongst other factors (Haug et al. et al. 2010), according to which the Burrowing Owl is 1993, Sheffield 1997). Although results of the present a common species in cities and tolerant to anthropic study have not demonstrated a negative impact of the environments. Burrowing Owl appears in different bird urbanization on Burrowing Owls, we cannot disregard lists of the Uberlândia (Silveira et al. 1989, Pimenta that the conservation of the species could be affected by 1993, Franchin & Marçal-Junior 2004, Franchin et al. the increase of human pressure, in the future. 2004) and, as demonstrated here, the species was able to The higher frequency of individuals and burrows in explore all urban biotopes sampled in this study. Some residential and green urban biotopes may be associated studies also suggest that Burrowing Owls are easily with a lower likelihood of disturbance in these areas behaviorally adjusted to humans, being able to colonize Revista Brasileira de Ornitologia 26(1): 2018 Influence of urbanization on Athene cunicularia Franco & Marçal-Junior Table 2. Number of individuals and burrows: main (refuges and nests) and satellite burrows of Burrowing Owl according to biotopes investigated in the urban area of Uberlândia, MG, Brazil. Percentage is the number of each burrow type in relation to the total number of burrows observed (n = 98 burrows). Main Biotopes Satellite Burrows Individuals Refuges Nests Residential 8 6 37 55 Green Urban Area 9 0 30 47 Commercial/Industrial 512 10 TOTAL 22 (22.4%) 7 (7.1%) 69 (70.5%) 112 Figure 4. Average depths of burrow of the Burrowing Owl Figure 3. Simple linear regression showing the positive according to biotopes (GUA = Green Urban Area; COM/ relationship between the number of satellite burrows and IND = Commercial/Industrial; RESID = Residential), the number of individuals of Burrowing Owl, in the city of with a significant difference between the Green Urban and Uberlândia (MG), Brazil. Commercial/Industrial Areas of Uberlândia (MG), Brazil. compared to the Commercial/Industrial biotope, which Smith 2003). The availability of burrows affects the choice had heavy traffic of vehicles and people, as well as low of habitat: the greater the number of burrows, the greater availability of land empty. The flow of vehicles and the probability of Burrowing Owls choosing it (Plumpton humans is considered to be the main cause of Burrowing & Lutz 1993, Desmond & Savidge 1999, Ronan 2002, Owl mortality (Silva 2002). On the other hand, the Poulin et al. 2005, Lantz et al. 2007). Burrowing Owls presence of empty lands may have favored the greater seemed to choose more areas corresponding to the occurrence of the species, as these unoccupied spaces Residential biotope, which presented greater numbers present favorable conditions for species survival (Forman of burrows (main ones and satellites) and, consequently, & Godron 1986, Blair 1996). It is worth mentioning that more individuals, probably because that biotope presented these areas present greater availability of food resources the most favorable characteristics for the species survival, due to the intense lighting near burrows, which attracts such as short grasses and greater food availability. In some beetles and other insects (Chipman et al. 2008). this study, deeper burrows were recorded in Residential The urban environment has few refuges and p laces and Green Urban Areas. Burrows are used for nesting, for breeding, feeding, resting and protection against refuge, to storage food and also may serve as a defense adverse climatic conditions such as rain or wind (Poulin mechanism. Accordingly, Burrowing Owls tend to dig et al. 2011). The Burrowing Owl does not dig their own deeper, especially in places with higher degrees of threats burrows, but takes advantage of previously dug burrows, (Thomsen 1971). We believe that behavior of digging modifying only their depths and widths (Belthoff & deeper is related to the type of biotope, like in Residential Revista Brasileira de Ornitologia 26(1): 2018 Influence of urbanization on Athene cunicularia Franco & Marçal-Junior Rabie P.A. & Euliss B.R. 2003. Effects of management practices and Green Urban Areas, biotopes with a probable higher on grassland birds: Burrowing Owls. Jamestown: Northern Prairie risk of predation by domestic animals and other potential Wildlife Research Center. predators. May be the greater the number of individuals, Delibes M., Blázquez M.C., Soriano L., Revilla E. & Godoy J.A. the greater will be the need for protection against possible 2011. High antipredatory efficiency of insular lizards: a warning threats, such as predators, that can use urban areas as signal of excessive specimen collection? PLoS ONE 6: e29312. Desmond M.J. & Savidge J.A. 1999. Satellite burrow use by Burrowing refuge (Griffin et al. 2017). 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Current status, distribution, and conservation of the Burrowing Owl (Speotyto cunicularia) in midwestern and Associate Editor: Carla S. Fontana. Revista Brasileira de Ornitologia 26(1): 2018 Influence of urbanization on Athene cunicularia Franco & Marçal-Junior APPENDIX I Classification of Burrowing Owl, Athene cunicularia: Adult female (A) and male (B); Juveniles (C) and chick (D), in urban environment. Photo authors: Felipe F. Franco (A & B); Phyllis Greenberg (C & D). A B C D Revista Brasileira de Ornitologia 26(1): 2018 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Ornithology Research Springer Journals

Influence of urbanization on the distribution and defense strategies of the Burrowing Owl Athene cunicularia in the city of Uberlândia, southeastern Brazil

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Revista Brasileira de Ornitologia 26(1): 1–8. ARTICLE March 2018 Influence of urbanization on the distribution and defense strategies of the Burrowing Owl Athene cunicularia in the city of Uberlândia, southeastern Brazil 1,2,3 2 Felipe Fina Franco & Oswaldo Marçal-Junior Graduate Program in Ecology and Conservation of Natural Resources, Institute of Biology, Federal University of Uberlândia, Campus Umuarama, Rua Ceará s/n, Bloco 2D, sala 34, Uberlândia, MG, 38400-902, Brazil. Laboratory of Ornithology and Bioacustics, Federal University of Uberlândia, Campus Umuarama, Rua Ceará s/n, Bloco 2D, sala 34, Uberlândia, MG, 38400-902, Brazil. Corresponding author: felipefinafranco@hotmail.com Received on 19 September 2017. Accepted on 19 January 2018. ABSTRACT: Urbanization causes drastic changes in habitat and species behavior. In birds, these changes influenced t he extinction of some species. The Burrowing Owl Athene cunicularia (Molina, 1782) (Aves: Strigiformes) has achieved some success in its adaptive process in anthropic environments. The main objective of this study was to measure distribution of this species in urban areas. The specific o bjectives were to quantify and compare the occurrence of this owl and its satellite burrows among urban biotopes; evaluate the importance of satellite burrows as a defense strategy and compare the depth of burrows in different biotopes. Field activities were carried out from August 2015 to November 2016. Sixty areas were sampled in different urban regions. The species was present in 29 of the 60 sites investigated, totaling 112 individuals, 88 adults, 14 young and 10 chicks; 98 burrows were recorded, from which 22 were refuges, seven nests and 67 satellite burrows. Residential and Urban Green Area biotopes had the highest number of individuals and burrows with a significant difference relative to the Commer cial/Industrial biotope. A greater number of individuals were found in areas with a high number of burrows showing a positive linear relationship between these variables. The burrows were deepest, on average, in Urban Green Area biotopes. We conclude that the species has a wide distribution in the city with significantly high numbers in the Residential biotope. This same tendency is verified for the distribution of burrows. In areas with a large number of individuals, the same was observed for the number of satellite burrows. Deeper burrows in the Urban Green Areas are perhaps due to the greater transit of people, one of the main features of this biotope and one of the major threats to the Burrowing Owls. KEY-WORDS: biotope, habitat, occurrence, satellite burrows, survival. INTRODUCTION having an important role in the food chain (Millennium Ecosystem Assessment 2005). In addition, they perform Urbanization can be defined as a process of anthropic functions like pollination and dispersal of fruits and seeds occupation that gradually transforms natural (Silva & Nakano 2008). environments and includes the presence of relatively Some of these birds live in urban environments, permanent human populations on the site (Marzluff such as Athene cunicularia (Molina, 1782), that is widely distributed throughout the Americas, from Canada et al. 2001). On a global scale, anthropic pressures have influenced t he structure and behavior of faunal to southern Argentina (Poulin et al. 2005, 2011). populations and communities, and also of ecosystems Burrowing Owls have preference for open habitats, in remnants of natural areas (Bradshaw & Holzapfel foraging and breeding in short, low-density vegetation 2006, Delibes et al. 2011). Human presence can lead to and mainly grasslands (Rebolo-Ifrán et al. 2017). These owls are common in Brazil and known for being urban population decline, persistence, or even the expansion of bird distributions (Sih et al. 2011). Furthermore, the dwellers, showing behavioral adjustments to anthropic- disturbances caused by anthropic actions seem to be altered environments (although they are commonly causing changes in the distribution and behavior of birds observed in natural areas) (Sick 1997, Motta-Junior and might also be leading many species to extinction & Alho 2000). Some populations are able to exploit human-made habitats with a preference for urban over (Silva & Nakano 2008). Many birds have adapted to the anthropic rural areas (natural grasslands and low-intensive agro- environment and their presence is important for pest pastoral lands) (Rebolo-Ifrán et al. 2017). Main causes control, such as predation of rats and insects, besides of mortality include collisions with vehicles and nest Influence of urbanization on Athene cunicularia Franco & Marçal-Junior destruction (Silva 2002). The behavioral responses of METHODS Burrowing Owls to threats can be easily recognized, such as the use of deep burrows, use of satellite burrows, flying Study area and data collection away in the presence of potential predators, making alarm calls, adopting threat postures and some type of attacks The municipality of U berlândia has about 669,000 (Coulombe 1971, Thomsen 1971, Fisher et al. 2004). habitants (IBGE 2016), with a total area of 4040 km in Burrowing Owls are present in many parts of the the state of Minas Gerais (MG), southeastern Brazil, from world and are considered one of the main predator which 219 km are urban. In areas surrounding the city, species of rodents in urban areas (Martins & Eagler 1990, the native vegetation was reduced to remnants of less than Sick 1997, Motta-Junior & Alho 2000). However, the 15% of the original cover, with evident reduction of the behavior of the species is affected by urbanization and it local fauna (Brito & Prudente 2005). is reported that the increase in vehicular traffic around We visited areas with a potential occurrence of the the nest produces an increase in the couple's waking species, typically with short grasses and wide spaces of time (Plumpton & Lutz 1993). Similarly, populations open areas (Coulombe 1971, Plumpton & Lutz 1993, of Burrowing Owls are under heavy pressure from Marks et al. 1999). Field activities were carried out from domestic animals, such as dogs and cats (Dechant et al. August 2015 to November 2016, with monthly data 2003, Rosenberg & Haley 2004, Moulton et al. 2006). collections along the day (from 7:00 h to 18:00 h) with These threats determine behavioral responses that include small interruptions, not every day of the month, and subterranean retreat, deeper burrows, the use of satellite totaling 2000 h of observation. burrows, the issuance of alarm calls, and dive-in-flight Sixty sites (with areas of about 33 m each) were attacks (Coulombe 1971, Thomsen 1971, Fisher et al. sampled in different parts of the city, 20 per urban biotope, 2004). It has also been described the use of mammalian and visited monthly. The minimum distance between sites manure, placed near the entrance of the burrow, to avoid was 200 m, in order to guarantee the independence of potential predators with bad odor (Martin 1973). the samples and considering the territorial behavior of the Burrows are the essential component of Burrowing studied species (Gaston 2003). These sites were selected Owl habitat: both natural and artificial burrows provide according to the potential occurrence of the Burrowing protection, shelter, and nests (Henny & Blus 1981). Owls with the help of satellite images obtained from the Burrowing Owls typically use burrows made by fossorial Google image bank of the city of Uberlândia (Google mammals, but also may use man-made structures, such Earth 5.1 2009) and also by direct field o bservations. All as cement culverts; cement, asphalt, or wood debris sites were georeferenced by taken a point in the middle piles; or openings beneath cement or asphalt pavement. using a Global Positioning System (GPS) and a map of Burrowing Owls exhibit high site fidelity, reusing burrows the city was made with these GPS points in the software year after year (Rich 1984, Feeney 1992). Once young QGIS 2.18.2 (Fig. 1). individuals learn to fly, the family group often moves Biotope refers to a certain living space distinct from from one burrow to another (Thomsen 1971). the others, endowed with environmental conditions Declines in populations of this species in North suitable for specific organisms (Sukopp & Weiler America called the attention of environmentalists 1988). The selected sites were classified a ccording to (Holroyd et al. 2001, Skeel et al. 2001, Warnock & Skeel the European Method for Mapping Biotopes: Urban 2004, Conway & Pardieck 2006) and, in Florida, the Green Areas, Residential and Commercial/Industrial Burrowing Owl had its status updated to threatened in (Sukopp & Weiler 1988, Weber & Bedê 1998). Urban the state red lists (Florida Fish and Wildlife Conservation Green Areas include urban parks, squares, sports Commission 2017). The aim of the present study was centers, theaters, universities, schools and airports, to determine the distribution and the abundance of the all places in which there is a high flow of people and a Burrowing Owl in urban areas of the city of Uberlândia, medium level of urbanization. The residential biotope is southeastern Brazil, by (1) evaluating the occurrence and characterized by the presence of houses, condominiums abundance of the species among different urban biotopes; and residential buildings, with less evident levels of (2) determining the occurrence and distribution of pollution and environmental disturbances; in addition, burrows (satellites, nests or refuges) per urban biotopes; this biotope has a lower flow of humans and ve hicles (3) evaluating different defense mechanisms, such as the (but with constant presence of domestic animals). The importance of satellite burrows, the relationship between Commercial/Industrial biotope includes open areas with the number of individuals and burrows; and the depth of short grasses, near places with intense commerce, such as the burrows in different biotopes, which are fundamental malls, industries or construction sites, with intense traffic aspects for conservation of the studied species in modified of vehicles and high level of urbanization. environments. Three visits were conducted to each site, totaling 180 Revista Brasileira de Ornitologia 26(1): 2018 Influence of urbanization on Athene cunicularia Franco & Marçal-Junior Figure 1. A map of the distribution of the sampled points for the Burrowing Owl occurrence, according to the investigated biotopes (Urban Green Area, Residential or Commercial/Industrial) in the urban area of Uberlândia (MG), Brazil. visits (60 visits in each biotope investigated). The relative biotopes we used the ANOVA One-Factor test. Tukey's abundance was calculated by counting individuals of test was used to determine which factor levels (urban the target species per site and the same was done for the biotope) differed from each other (Zar 2010). Another burrows. Individuals were classified a ccording to gender ANOVA test was used to evaluate the differences in (only adults) (Zarn 1974) and age group (adults, chicks burrow depth by biotope. and juveniles) (Appendix I). Burrows were classified as To evaluate the correlation between number of main or satellite. Main burrows were subdivided by nests individuals and burrows we performed a simple linear (in which chicks or eggs were present) and refuges (in regression. Values were square root transformed for which only adults were present). Satellite burrows were normality adjustment (Zar 2010). All statistical analyzes represented by non-inhabited burrows near the main were performed using the Systat 10.2 software, with a ones, and are used as a defense mechanism against threats, significance level of  = 0.05 (Zar 2010) and graphs were in which individuals rotate between burrows in order to built using Illustrator 21.1.0. confuse predators (Henny & Blus 1981, Desmond & Savidge 1999). Some burrows were lost due to human action. RESULTS To measure the depth of the burrows we used a digital measuring tape (Bosch GLM30) 5 m long. Only Distribution, occurrence and abundance burrows that we could reach without causing stress (absence of individuals) or nests without the presence of The species was found in 29 out of the 60 sampled sites chicks, were measured. (48%). In total, 98 burrows were registered, with a mean of 3.14 burrows per point, with 29 main burrows (22 Data analysis refuges and seven nests) and 69 satellite burrows. We recorded 112 individuals (Table 1). Homogeneity tests of variances and normality of the sampled data were performed using a Lilliefors test and by Distribution and occurrence by biotopes evaluating the data distribution in scatter plots. Sample data transformations (three times in the Variance Analysis, Residential biotope points showed the highest number of individuals (n = 55) followed by Green Urban Area in addition to the Linear Regression) were performed by square rooting values, which were necessary due to the points (n = 47) and Commercial/Industrial Area points (n non-normality distribution of the sampling data (Zar = 10). The largest number of individuals found in a single 2010). To determine the differences in Burrowing Owl point was recorded in a Residential biotope (n = 8). A abundance and number of burrows according to urban mean of three individuals per point were recorded in the Revista Brasileira de Ornitologia 26(1): 2018 Influence of urbanization on Athene cunicularia Franco & Marçal-Junior Table 1. Number of individuals of Burrowing Owl, by age group (adults, juveniles and chicks) and gender (male and female) in the biotopes investigated in the urban area of Uberlândia (MG), Brazil. Adults Biotopes Chicks Juveniles Total Male Female Residential 21 22 9 3 55 Green Urban Area 18 18 4 7 47 Commercial/Industrial 36 1 0 10 TOTAL 42 46 14 10 112 Residential biotope, two in Green Urban Area and 0.5 in Commercial/Industrial (F = 4.2, P = 0.020, Fig. 2A), (2,57) with a significant difference between the Residential and Commercial/Industrial biotopes (P < 0.016). Distribution and occurrence of burrows by biotopes We found 51 burrows in the Residential biotope, 39 in Green Urban Area and 8 in Commercial/Industrial (F (2,57) = 3.19, P = 0.048, Fig. 2B), with a significant difference between Residential and Commercial/Industrial (Tukey's test; P < 0.040). Relationship between satellite burrows and number of individuals In general, large numbers of satellite burrows were found in points with large number of individuals, with a positive Figure 2. (A) Mean of individuals of Burrowing Owl per point linear relationship between the two variables (F = distributed according to the biotopes (G.U.A = Green Urban (1,58) 428.89, P < 0.001, R > 0.88) (Fig. 3) (Table 2). Area; COM/IND = Commercial/Industrial) in Uberlândia (MG), Brazil; (B) Mean number of burrows per point, showing a relationship between burrows (refuges, satellites and nests) Depths of burrows in the urban biotopes and biotopes (G.U.A = Green Urban Area; COM/IND = Commercial/Industrial) of the Burrowing Owl in Uberlândia Thirty-four depths of burrows were measured. The (MG), Brazil. Confidence intervals were considered for P < highest mean was observed in the Green Urban Area 0.05. biotope, reaching a maximum depth of 3.5 m. There was a significant difference between the three biotopes (F (2,17) different human-altered habitats (Sih et al. 2011, Sol et al. = 4.05, P < 0.030, Fig. 4), with the greatest depths in the 2013, Rebolo-Ifrán et al. 2017). On the other hand, some Green Urban Area (P = 0.049). studies indicate that urbanization leads to the population decline of Burrowing Owls (Millsap & Bear 2000, Jones DISCUSSION & Bock 2002, Chipman et al. 2008). This decline is attributed to the loss of habitat to cultivation and other The results obtained corroborated other studies (Haug et land use activities, predation by domestic animals and al. 1993, Holmes 1998, Chipman et al. 2008, Berardelli human persecution, amongst other factors (Haug et al. et al. 2010), according to which the Burrowing Owl is 1993, Sheffield 1997). Although results of the present a common species in cities and tolerant to anthropic study have not demonstrated a negative impact of the environments. Burrowing Owl appears in different bird urbanization on Burrowing Owls, we cannot disregard lists of the Uberlândia (Silveira et al. 1989, Pimenta that the conservation of the species could be affected by 1993, Franchin & Marçal-Junior 2004, Franchin et al. the increase of human pressure, in the future. 2004) and, as demonstrated here, the species was able to The higher frequency of individuals and burrows in explore all urban biotopes sampled in this study. Some residential and green urban biotopes may be associated studies also suggest that Burrowing Owls are easily with a lower likelihood of disturbance in these areas behaviorally adjusted to humans, being able to colonize Revista Brasileira de Ornitologia 26(1): 2018 Influence of urbanization on Athene cunicularia Franco & Marçal-Junior Table 2. Number of individuals and burrows: main (refuges and nests) and satellite burrows of Burrowing Owl according to biotopes investigated in the urban area of Uberlândia, MG, Brazil. Percentage is the number of each burrow type in relation to the total number of burrows observed (n = 98 burrows). Main Biotopes Satellite Burrows Individuals Refuges Nests Residential 8 6 37 55 Green Urban Area 9 0 30 47 Commercial/Industrial 512 10 TOTAL 22 (22.4%) 7 (7.1%) 69 (70.5%) 112 Figure 4. Average depths of burrow of the Burrowing Owl Figure 3. Simple linear regression showing the positive according to biotopes (GUA = Green Urban Area; COM/ relationship between the number of satellite burrows and IND = Commercial/Industrial; RESID = Residential), the number of individuals of Burrowing Owl, in the city of with a significant difference between the Green Urban and Uberlândia (MG), Brazil. Commercial/Industrial Areas of Uberlândia (MG), Brazil. compared to the Commercial/Industrial biotope, which Smith 2003). The availability of burrows affects the choice had heavy traffic of vehicles and people, as well as low of habitat: the greater the number of burrows, the greater availability of land empty. The flow of vehicles and the probability of Burrowing Owls choosing it (Plumpton humans is considered to be the main cause of Burrowing & Lutz 1993, Desmond & Savidge 1999, Ronan 2002, Owl mortality (Silva 2002). On the other hand, the Poulin et al. 2005, Lantz et al. 2007). Burrowing Owls presence of empty lands may have favored the greater seemed to choose more areas corresponding to the occurrence of the species, as these unoccupied spaces Residential biotope, which presented greater numbers present favorable conditions for species survival (Forman of burrows (main ones and satellites) and, consequently, & Godron 1986, Blair 1996). It is worth mentioning that more individuals, probably because that biotope presented these areas present greater availability of food resources the most favorable characteristics for the species survival, due to the intense lighting near burrows, which attracts such as short grasses and greater food availability. In some beetles and other insects (Chipman et al. 2008). this study, deeper burrows were recorded in Residential The urban environment has few refuges and p laces and Green Urban Areas. Burrows are used for nesting, for breeding, feeding, resting and protection against refuge, to storage food and also may serve as a defense adverse climatic conditions such as rain or wind (Poulin mechanism. Accordingly, Burrowing Owls tend to dig et al. 2011). The Burrowing Owl does not dig their own deeper, especially in places with higher degrees of threats burrows, but takes advantage of previously dug burrows, (Thomsen 1971). We believe that behavior of digging modifying only their depths and widths (Belthoff & deeper is related to the type of biotope, like in Residential Revista Brasileira de Ornitologia 26(1): 2018 Influence of urbanization on Athene cunicularia Franco & Marçal-Junior Rabie P.A. & Euliss B.R. 2003. Effects of management practices and Green Urban Areas, biotopes with a probable higher on grassland birds: Burrowing Owls. Jamestown: Northern Prairie risk of predation by domestic animals and other potential Wildlife Research Center. predators. May be the greater the number of individuals, Delibes M., Blázquez M.C., Soriano L., Revilla E. & Godoy J.A. the greater will be the need for protection against possible 2011. High antipredatory efficiency of insular lizards: a warning threats, such as predators, that can use urban areas as signal of excessive specimen collection? PLoS ONE 6: e29312. Desmond M.J. & Savidge J.A. 1999. Satellite burrow use by Burrowing refuge (Griffin et al. 2017). 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Current status, distribution, and conservation of the Burrowing Owl (Speotyto cunicularia) in midwestern and Associate Editor: Carla S. Fontana. Revista Brasileira de Ornitologia 26(1): 2018 Influence of urbanization on Athene cunicularia Franco & Marçal-Junior APPENDIX I Classification of Burrowing Owl, Athene cunicularia: Adult female (A) and male (B); Juveniles (C) and chick (D), in urban environment. Photo authors: Felipe F. Franco (A & B); Phyllis Greenberg (C & D). A B C D Revista Brasileira de Ornitologia 26(1): 2018

Journal

Ornithology ResearchSpringer Journals

Published: Mar 1, 2018

Keywords: biotope; habitat; occurrence; satellite burrows; survival

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