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Behavioral responses of urban birds to human disturbance in urban parks at Curitiba, Paraná (Brazil)

Behavioral responses of urban birds to human disturbance in urban parks at Curitiba, Paraná (Brazil) Revista Brasileira de Ornitologia 26(2): 77–81. ARTICLE June 2018 Behavioral responses of urban birds to human disturbance in urban parks at Curitiba, Paraná (Brazil) 1,2 2,4 2,3 Thays Verônica Prestes , Lilian Tonelli Manica & André de Camargo Guaraldo Graduação em Ciências Biológicas, Universidade Federal do Paraná, Curitiba, PR, Brazil. Laboratório de Ecologia Comportamental e Ornitologia (LECO), Departamento de Zoologia, Universidade Federal do Paraná, Curitiba, PR, Brazil. Programa de Pós-graduação em Ecologia e Conservação, Setor de Ciências Biológicas, Universidade Federal do Paraná, Curitiba, PR, Brazil. Corresponding author: lilianmanica@gmail.com Received on 13 January 2018. Accepted on 25 May 2018. ABSTRACT: Proximity to humans can influence behaviors that are essential in birds' life, such as breeding, foraging and flight. In urban parks, which are important natural shelters to birds, human activity varies broadly in time such that attentiveness and escaping behavior of birds may be intensified as humans' density increases. In this study, we tested this hypothesis in six urban parks at Curitiba, southern Brazil, using three common bird species as models, the Rufous Hornero (Furnarius rufus), the Southern Lapwing (Vanellus chilensis) and the Rufous-bellied Thrush (Turdus rufiventris). Specifically, we tested if foraging rate, alert distance (AD), flight initiation distance (FID) and flight distance (FD) were related to human density at birds' surroundings. We found no influence of humans on birds foraging rate, whereas AD, FID and FD decreased with human density in the area. We also found differences in birds escaping strategy; “flying” strategy was associated with higher AD, FID and FD than “walking”. Results also indicate that humans' presence temporally affected birds' vigilance and flight responses, evident through t heir constant foraging rate irrespective of human density, i.e. increased tolerance to human proximity. Our study provides evidence of behavioral plasticity of the model species to the intensity of human use of their living area, which also highlights the importance of further efforts in creating refuges within urban parks to minimize negative anthropic impacts on urban species. KEY-WORDS: approaching experimental trial, escaping strategy, flight initiation distance, foraging rate, human density. INTRODUCTION individuals and species less sensitive to urbanization. The escape behavior to human approach reflects a Many bird species are sensitive to environmental change, bird innate response to guarantee survival. Individual but several can cope with anthropic activities. Thus, parks responses involve an optimal decision-making that and other green areas become important shelter especially maximizes foraging and daily general activities (e.g. to birds in human-altered environments (Fernández- mating and nesting) while reducing any potential threat (Blumstein et al. 2003, Piratelli et al. 2015). Three Juricic et al. 2001), because ecological and environmental conditions may match with the natural contexts where important metrics to assess an individual habituation these species have evolved. However, human use of green and risk avoidance agility are the alert distance (AD), areas for leisure or touristic activities can also cause flight initiation distance (FID) and flight distance (FD). profound impacts in wildlife (Collins-Kreiner et al. The first indicates birds' visual and auditory orientation when detecting an approaching threat (Blumstein 2006, 2013). For instance, the presence of humans may cause foraging area reduction and increasing stress hormone Weston et al. 2012). Specifically, t he alert state in birds levels in urban animals that can affect parental care (e.g., is easily recognized through behaviors like head raise Haematopus ostralegus, Verhulst et al. 2001), hatching (Whitfield et al. 2008), continuous surroundings scan success and chick development (e.g., Opisthocomus hoazin, (Schlacher et al. 2013) and momentarily interruption of activities. The second in dicates the distance in relation to Mullner et al. 2004 and Pygoscelis adeliae, Giese 1996), high mortality rates (Blumstein 2006) and, ultimately, a potential threat at which the individual begins to escape local species extinction. Even though selection has favored by walking or flying away (Cooper-Jr. & Pérez-Mellado agile escape behaviors in birds to overcome potential 2011), and the third represents the actual distance threats (e.g. predators, Ydenberg & Dill 1986), individual travelled for escaping. Optimized alertness and escape responses, measured habituation to human co-occurrence can be decisive for survival and may represent an important filter selecting as AD, FID and FD, may allow birds to accomplish their Urban birds responses to human disturbance Prestes et al. daily activities in a non-ideal condition for many species. represent human density at each trial in the analyses. We Indeed, birds exposed to human proximity tend to have ensured variable human density values across all samples by collecting data both in weekdays and weekends. lower AD, FID and FD, indicating tolerance to human approach likely due to habituation (Miller et al. 2001, During five minutes of observation we calculated each individual foraging effort as the number of pecks/min, Ikuta & Blumnstein 2003, Cooper-Jr. & Pérez-Mellado irrespective of their success in each capturing attempt. 2011). However, even low levels of human disturbance We conducted an approaching experiment by can be threatening to birds (Bötsch et al. 2017). For that walking towards each bird at a constant walking pace reason, these metrics may allow measuring the impacts (0.5–1.0 m/s) in a straight trajectory. We then marked of the human disturbance in birds living in a given area and measured with a measuring tape the researcher and how these animals cope with it. To better understand position when the bird displayed the alert behavior how urban birds deal with human proximity, we (AD) and when it walked or flew away (FID, Fig. 1). experimentally tested the hypothesis that birds respond We acquired FD by measuring the distance between the to humans' presence through shifting AD, FID, FD, researcher position when the bird initiated its flight and and their foraging rate in correlation to the amount of the refuge or landing position (Fig. 1). To standardize all humans that occupy or approach to their foraging areas. experimental trials, we set the researcher initial distance To do so, we had as models three common ground (ID) to the bird before any approach to be of at least 20 m foraging urban species, the Rufous Hornero (Furnarius (Fig. 1) and run all trials in non-rainy days. Since subjects rufus), the Southern Lapwing (Vanellus chilensis) and the were unmarked, we run the experiments in alternated Rufous-bellied Thrush (Turdus rufiventris). Considering days and local regions within each green area to avoid urban birds may habituate to humans' presence (Miller et sampling each individual repetitively and to prevent birds al. 2001, Ikuta & Blumnstein 2003, Cooper-Jr. & Pérez- to get habituated to the experiment. To avoid biases, the Mellado 2011), in days with denser human population in same researcher (T.V.P .) made all trials. urban green areas we expected that these birds would thus have lower AD, FID, and FD. In addition, increasing Statistical analysis number of people using the green areas would reduce the time window for food search by birds since they would We tested data for normality using Shapiro-Wilk test have to spend more time in alert posture than foraging. and transformed AD, FID, FD and foraging rate to their Therefore, we expected an inverse relationship between square root to approximate to a normal distribution. foraging rate and human density. Because AD, FID, and FD were correlated (AD-FID, r = 0.77; AD-FD, r = 0.54, and FID-FD, r = 0.64; P < 0.001 and df = 129 in all cases), we included them in a METHODS principal component analysis (PCA) and used the first principal component (PC1, explained variance = 77%) as Study area response variable. Higher PC1 values represented lower values of AD, FID and FD (loadings: -0.40, -0.50 and We collected data in 25 sampling days from August -0.77, correlations with PC1: -0.77, -0.85 and -0.93, to September 2016, in six green areas at Curitiba, the respectively). most populous city in Paraná state, south Brazil: Jardim We used two Analysis of Covariance (ANCOVA) o o Botânico (25 26'31''S; 49 14'27''W), Parque Barigui to test for the relationship between (i) PC1 and human o o (25 25'32''S; 49 18'58''W), Parque São Lourenço density and escape strategy (walking or flying), and (ii) o o o (25 23'13''S; 49 16'10''W), Passeio Público (25 25'32''S; between foraging rate and human density. We validated 49 16'11''W), Campus Centro Politécnico of the o o Universidade Federal do Paraná (25 27'6''S; 49 13'55''W) and Fazenda Experimental Canguiri of the Universidade o o Federal do Paraná (25 27'34''S; 49 15'54''W). Behavioral observations and approaching experiment We searched for individuals of the three model-species Figure 1. Schematic representation of recorded distances during foraging in each green area. We counted the number of approaching experiments to the birds. Dashed line indicates humans within a sampling plot with 20 m radius (1256.64 bird movement trajectory. ID: researcher initial distance; AD: m ) around each spotted bird either before and after bird alert distance; FID: flight initiation distance; and FD: each observation trial and used their average number to flight distance. Revista Brasileira de Ornitologia 26(2): 2018 Urban birds responses to human disturbance Prestes et al. Table 1. Foraging rate, alert distance (AD), flight initiation distance (FID) and flight distance (FD) recorded for each bird species in urban parks at Curitiba, Brazil. Values are mean ± SD. Foraging rate Species Sample size AD (m) FID (m) FD (m) (pecks/min) Rufous Hornero 51 44.6 ± 29.8 4.7 ± 1.98 2.6 ± 1.6 5.6 ± 5.5 Rufous-bellied Thrush 35 24.7 ± 21 6.5 ± 2.4 4.2 ± 2.3 7.9 ± 5.5 Southern Lapwing 45 12.3 ±13.6 7.9 ± 3.3 5.3 ± 3.3 8.3 ± 3.8 the models by plotting residuals versus fitted va lues. We 3). Altogether, this indicates that AD, FID and FD values run all statistical analyses in R 3.4.2 (R Core Team 2016). were higher when birds escaped on the wing, meaning that when humans' density was high, birds preferred walking instead of flying escapes, thus allowing closer RESULTS approach of the observer and evading to a nearer refuge as opposed to when humans were denser in the area and We made 133 records of foraging rate and approaching birds avoided their proximity by flying to a farther refuge. experiments to individuals of the three species: 51 Rufous Horneros, 45 Southern Lapwings and 35 Rufous-bellied Thrushes. Foraging rates were unrelated to human density ( ± SE = -0.009 ± 0.011, n = 131, t = -0.84, P = 0.40), indicating lack of human influence on food- searching behavior by birds (Fig. 2). We found variation in AD, FID and FD between species (Table 1; Fig. 3 left), supporting the inclusion of species as an additional fixed effect term in the models. PC1 was positively related to human density ( ± SE = 0.04 ± 0.01, n = 131, t = 4.09, P < 0.0001, Fig. 3), and indicated that AD, FID and FD reduced as human density increased. In other words, as the number of humans increased on birds surroundings, consequently reducing the area free of people, birds started escaping at shorter distances, but went to closer distances to the observer than in scenarios of low density Human density (humans/sampling plot) of humans. PC1 values were smaller when birds flew to escape ( ± SE = -1.04 ± 0.16, n = 131, t = -6.46, P < Figure 2. Bird's foraging rate in relation to human density per flight 0.0001) in comparison to the walking escape strategy (Fig. sampling plot (1256.64 m ) drawn with birds at its center. Figure 3. First principal component scores (PC1) of a Principal Component Analyses including AD, FID and FD in relation to humans' density per sampling plot (1256.64 m ; left; Rufous Hornero: solid line; Southern Lapwing: dashed line; Rufous-bellied Thrush: dotted line) and to escape strategy (right). Higher values of PC1 represents lower AD, FID and FD. Revista Brasileira de Ornitologia 26(2): 2018 Urban birds responses to human disturbance Prestes et al. DISCUSSION Escaping from an imminent threat requires prompt muscular response. In birds, flying is the fastest way of moving away, but also more energy demanding than In this study we tested the hypothesis that individuals of Rufous Horneros, Southern Lapwings and Rufous- running (Harrison & Roberts 2000). For this reason, bellied Thrushes in urban parks would a djust their birds should use flight over running for escaping solely foraging and escaping behavior according to the number when the risk is higher, thus allowing a faster response and reaching the farthest safe distances from the threat, as of humans on their proximity. We showed that birds of supported by our results. the three studied species kept foraging at the same rate irrespective of humans' density. Nevertheless, AD, FID Survival in urban habitats requires that birds cope and FD were shorter when more humans were at bird's with frequent interactions with humans, which ultimately surroundings, situation in which birds allowed a closer lead to birds becoming more tolerant to that. Despite of that, our results show that syntopy with humans ultimately approach of the observer and flew to a closer safe-distance affects birds' foraging strategy and always result in birds in the approaching experimental trials. The unpredicted result of human density unaffecting escaping using a plastic response that varies according to birds' foraging rate reveals a few plausible strategies birds human's density in the surrounding areas. By that, it is adopt to survive in urban environments. Bird hunting obvious that living in urban parks causes inherent stress responses in birds (e.g. raised heart rate, and escaping and trapping are illegal activities in Brazil (Brasil 1967), flight, Steven et al. 2011), which may ultimately affect therefore urban birds could have been associating humans' approximation as a non-threatening behavior (e.g. individual fitness and population survival. Therefore, we highlight that to improve the chances of native urban- Blumstein 2006, Weston et al. 2012, Guay et al. 2013), inhabitant bird species conservation it is important to ultimately leading to steady foraging rate. Furthermore, ensure that parks have human-free areas, in which birds the reduction on their adverse reactions to humans may could find refuge for foraging and resting especially in result from a foraging strategy optimized for ensuring days when the density of visitors increases such as during proper spatial and temporal exploration of resources weekends. in human populated habitats. When high number of humans occupy the parks, foraging may be hampered by the restricted amount of unoccupied foraging areas. To ACKNOWLEDGEMENTS overcome this problem, our data suggest that urban birds maximize their foraging efforts b y keep searching for food Authors thank a grant by CNPq to L.T.M. (455908/2014- despite of increased human proximity. This coincides to 1), CAPES for a post-doctoral fellowship to A.C.G. previous findings that birds become more tolerant to (PNPD-1459754), and volunteer field assistants. people when human encounter events are more frequent (Samia et al. 2015), but our results add that this occur even when the variation of encounter rates occurs REFERENCES within the same location. In other words, birds sustain constant foraging rates through shifting AD and FID to Blumstein D.T. 2006. Developing an evolutionary ecology of fear: their minimum when human's density increases, thus how life history and natural history traits affect disturbance expressing a finer trade-off equilibrium between energy tolerance in birds. Animal Behaviour 71: 389–399. intake and safety, extending to at least these three tropical Blumstein D.T., Anthony L.L., Harcourt R. & Ross G. 2003. 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Behavioral responses of urban birds to human disturbance in urban parks at Curitiba, Paraná (Brazil)

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Revista Brasileira de Ornitologia 26(2): 77–81. ARTICLE June 2018 Behavioral responses of urban birds to human disturbance in urban parks at Curitiba, Paraná (Brazil) 1,2 2,4 2,3 Thays Verônica Prestes , Lilian Tonelli Manica & André de Camargo Guaraldo Graduação em Ciências Biológicas, Universidade Federal do Paraná, Curitiba, PR, Brazil. Laboratório de Ecologia Comportamental e Ornitologia (LECO), Departamento de Zoologia, Universidade Federal do Paraná, Curitiba, PR, Brazil. Programa de Pós-graduação em Ecologia e Conservação, Setor de Ciências Biológicas, Universidade Federal do Paraná, Curitiba, PR, Brazil. Corresponding author: lilianmanica@gmail.com Received on 13 January 2018. Accepted on 25 May 2018. ABSTRACT: Proximity to humans can influence behaviors that are essential in birds' life, such as breeding, foraging and flight. In urban parks, which are important natural shelters to birds, human activity varies broadly in time such that attentiveness and escaping behavior of birds may be intensified as humans' density increases. In this study, we tested this hypothesis in six urban parks at Curitiba, southern Brazil, using three common bird species as models, the Rufous Hornero (Furnarius rufus), the Southern Lapwing (Vanellus chilensis) and the Rufous-bellied Thrush (Turdus rufiventris). Specifically, we tested if foraging rate, alert distance (AD), flight initiation distance (FID) and flight distance (FD) were related to human density at birds' surroundings. We found no influence of humans on birds foraging rate, whereas AD, FID and FD decreased with human density in the area. We also found differences in birds escaping strategy; “flying” strategy was associated with higher AD, FID and FD than “walking”. Results also indicate that humans' presence temporally affected birds' vigilance and flight responses, evident through t heir constant foraging rate irrespective of human density, i.e. increased tolerance to human proximity. Our study provides evidence of behavioral plasticity of the model species to the intensity of human use of their living area, which also highlights the importance of further efforts in creating refuges within urban parks to minimize negative anthropic impacts on urban species. KEY-WORDS: approaching experimental trial, escaping strategy, flight initiation distance, foraging rate, human density. INTRODUCTION individuals and species less sensitive to urbanization. The escape behavior to human approach reflects a Many bird species are sensitive to environmental change, bird innate response to guarantee survival. Individual but several can cope with anthropic activities. Thus, parks responses involve an optimal decision-making that and other green areas become important shelter especially maximizes foraging and daily general activities (e.g. to birds in human-altered environments (Fernández- mating and nesting) while reducing any potential threat (Blumstein et al. 2003, Piratelli et al. 2015). Three Juricic et al. 2001), because ecological and environmental conditions may match with the natural contexts where important metrics to assess an individual habituation these species have evolved. However, human use of green and risk avoidance agility are the alert distance (AD), areas for leisure or touristic activities can also cause flight initiation distance (FID) and flight distance (FD). profound impacts in wildlife (Collins-Kreiner et al. The first indicates birds' visual and auditory orientation when detecting an approaching threat (Blumstein 2006, 2013). For instance, the presence of humans may cause foraging area reduction and increasing stress hormone Weston et al. 2012). Specifically, t he alert state in birds levels in urban animals that can affect parental care (e.g., is easily recognized through behaviors like head raise Haematopus ostralegus, Verhulst et al. 2001), hatching (Whitfield et al. 2008), continuous surroundings scan success and chick development (e.g., Opisthocomus hoazin, (Schlacher et al. 2013) and momentarily interruption of activities. The second in dicates the distance in relation to Mullner et al. 2004 and Pygoscelis adeliae, Giese 1996), high mortality rates (Blumstein 2006) and, ultimately, a potential threat at which the individual begins to escape local species extinction. Even though selection has favored by walking or flying away (Cooper-Jr. & Pérez-Mellado agile escape behaviors in birds to overcome potential 2011), and the third represents the actual distance threats (e.g. predators, Ydenberg & Dill 1986), individual travelled for escaping. Optimized alertness and escape responses, measured habituation to human co-occurrence can be decisive for survival and may represent an important filter selecting as AD, FID and FD, may allow birds to accomplish their Urban birds responses to human disturbance Prestes et al. daily activities in a non-ideal condition for many species. represent human density at each trial in the analyses. We Indeed, birds exposed to human proximity tend to have ensured variable human density values across all samples by collecting data both in weekdays and weekends. lower AD, FID and FD, indicating tolerance to human approach likely due to habituation (Miller et al. 2001, During five minutes of observation we calculated each individual foraging effort as the number of pecks/min, Ikuta & Blumnstein 2003, Cooper-Jr. & Pérez-Mellado irrespective of their success in each capturing attempt. 2011). However, even low levels of human disturbance We conducted an approaching experiment by can be threatening to birds (Bötsch et al. 2017). For that walking towards each bird at a constant walking pace reason, these metrics may allow measuring the impacts (0.5–1.0 m/s) in a straight trajectory. We then marked of the human disturbance in birds living in a given area and measured with a measuring tape the researcher and how these animals cope with it. To better understand position when the bird displayed the alert behavior how urban birds deal with human proximity, we (AD) and when it walked or flew away (FID, Fig. 1). experimentally tested the hypothesis that birds respond We acquired FD by measuring the distance between the to humans' presence through shifting AD, FID, FD, researcher position when the bird initiated its flight and and their foraging rate in correlation to the amount of the refuge or landing position (Fig. 1). To standardize all humans that occupy or approach to their foraging areas. experimental trials, we set the researcher initial distance To do so, we had as models three common ground (ID) to the bird before any approach to be of at least 20 m foraging urban species, the Rufous Hornero (Furnarius (Fig. 1) and run all trials in non-rainy days. Since subjects rufus), the Southern Lapwing (Vanellus chilensis) and the were unmarked, we run the experiments in alternated Rufous-bellied Thrush (Turdus rufiventris). Considering days and local regions within each green area to avoid urban birds may habituate to humans' presence (Miller et sampling each individual repetitively and to prevent birds al. 2001, Ikuta & Blumnstein 2003, Cooper-Jr. & Pérez- to get habituated to the experiment. To avoid biases, the Mellado 2011), in days with denser human population in same researcher (T.V.P .) made all trials. urban green areas we expected that these birds would thus have lower AD, FID, and FD. In addition, increasing Statistical analysis number of people using the green areas would reduce the time window for food search by birds since they would We tested data for normality using Shapiro-Wilk test have to spend more time in alert posture than foraging. and transformed AD, FID, FD and foraging rate to their Therefore, we expected an inverse relationship between square root to approximate to a normal distribution. foraging rate and human density. Because AD, FID, and FD were correlated (AD-FID, r = 0.77; AD-FD, r = 0.54, and FID-FD, r = 0.64; P < 0.001 and df = 129 in all cases), we included them in a METHODS principal component analysis (PCA) and used the first principal component (PC1, explained variance = 77%) as Study area response variable. Higher PC1 values represented lower values of AD, FID and FD (loadings: -0.40, -0.50 and We collected data in 25 sampling days from August -0.77, correlations with PC1: -0.77, -0.85 and -0.93, to September 2016, in six green areas at Curitiba, the respectively). most populous city in Paraná state, south Brazil: Jardim We used two Analysis of Covariance (ANCOVA) o o Botânico (25 26'31''S; 49 14'27''W), Parque Barigui to test for the relationship between (i) PC1 and human o o (25 25'32''S; 49 18'58''W), Parque São Lourenço density and escape strategy (walking or flying), and (ii) o o o (25 23'13''S; 49 16'10''W), Passeio Público (25 25'32''S; between foraging rate and human density. We validated 49 16'11''W), Campus Centro Politécnico of the o o Universidade Federal do Paraná (25 27'6''S; 49 13'55''W) and Fazenda Experimental Canguiri of the Universidade o o Federal do Paraná (25 27'34''S; 49 15'54''W). Behavioral observations and approaching experiment We searched for individuals of the three model-species Figure 1. Schematic representation of recorded distances during foraging in each green area. We counted the number of approaching experiments to the birds. Dashed line indicates humans within a sampling plot with 20 m radius (1256.64 bird movement trajectory. ID: researcher initial distance; AD: m ) around each spotted bird either before and after bird alert distance; FID: flight initiation distance; and FD: each observation trial and used their average number to flight distance. Revista Brasileira de Ornitologia 26(2): 2018 Urban birds responses to human disturbance Prestes et al. Table 1. Foraging rate, alert distance (AD), flight initiation distance (FID) and flight distance (FD) recorded for each bird species in urban parks at Curitiba, Brazil. Values are mean ± SD. Foraging rate Species Sample size AD (m) FID (m) FD (m) (pecks/min) Rufous Hornero 51 44.6 ± 29.8 4.7 ± 1.98 2.6 ± 1.6 5.6 ± 5.5 Rufous-bellied Thrush 35 24.7 ± 21 6.5 ± 2.4 4.2 ± 2.3 7.9 ± 5.5 Southern Lapwing 45 12.3 ±13.6 7.9 ± 3.3 5.3 ± 3.3 8.3 ± 3.8 the models by plotting residuals versus fitted va lues. We 3). Altogether, this indicates that AD, FID and FD values run all statistical analyses in R 3.4.2 (R Core Team 2016). were higher when birds escaped on the wing, meaning that when humans' density was high, birds preferred walking instead of flying escapes, thus allowing closer RESULTS approach of the observer and evading to a nearer refuge as opposed to when humans were denser in the area and We made 133 records of foraging rate and approaching birds avoided their proximity by flying to a farther refuge. experiments to individuals of the three species: 51 Rufous Horneros, 45 Southern Lapwings and 35 Rufous-bellied Thrushes. Foraging rates were unrelated to human density ( ± SE = -0.009 ± 0.011, n = 131, t = -0.84, P = 0.40), indicating lack of human influence on food- searching behavior by birds (Fig. 2). We found variation in AD, FID and FD between species (Table 1; Fig. 3 left), supporting the inclusion of species as an additional fixed effect term in the models. PC1 was positively related to human density ( ± SE = 0.04 ± 0.01, n = 131, t = 4.09, P < 0.0001, Fig. 3), and indicated that AD, FID and FD reduced as human density increased. In other words, as the number of humans increased on birds surroundings, consequently reducing the area free of people, birds started escaping at shorter distances, but went to closer distances to the observer than in scenarios of low density Human density (humans/sampling plot) of humans. PC1 values were smaller when birds flew to escape ( ± SE = -1.04 ± 0.16, n = 131, t = -6.46, P < Figure 2. Bird's foraging rate in relation to human density per flight 0.0001) in comparison to the walking escape strategy (Fig. sampling plot (1256.64 m ) drawn with birds at its center. Figure 3. First principal component scores (PC1) of a Principal Component Analyses including AD, FID and FD in relation to humans' density per sampling plot (1256.64 m ; left; Rufous Hornero: solid line; Southern Lapwing: dashed line; Rufous-bellied Thrush: dotted line) and to escape strategy (right). Higher values of PC1 represents lower AD, FID and FD. Revista Brasileira de Ornitologia 26(2): 2018 Urban birds responses to human disturbance Prestes et al. DISCUSSION Escaping from an imminent threat requires prompt muscular response. In birds, flying is the fastest way of moving away, but also more energy demanding than In this study we tested the hypothesis that individuals of Rufous Horneros, Southern Lapwings and Rufous- running (Harrison & Roberts 2000). For this reason, bellied Thrushes in urban parks would a djust their birds should use flight over running for escaping solely foraging and escaping behavior according to the number when the risk is higher, thus allowing a faster response and reaching the farthest safe distances from the threat, as of humans on their proximity. We showed that birds of supported by our results. the three studied species kept foraging at the same rate irrespective of humans' density. Nevertheless, AD, FID Survival in urban habitats requires that birds cope and FD were shorter when more humans were at bird's with frequent interactions with humans, which ultimately surroundings, situation in which birds allowed a closer lead to birds becoming more tolerant to that. Despite of that, our results show that syntopy with humans ultimately approach of the observer and flew to a closer safe-distance affects birds' foraging strategy and always result in birds in the approaching experimental trials. The unpredicted result of human density unaffecting escaping using a plastic response that varies according to birds' foraging rate reveals a few plausible strategies birds human's density in the surrounding areas. By that, it is adopt to survive in urban environments. Bird hunting obvious that living in urban parks causes inherent stress responses in birds (e.g. raised heart rate, and escaping and trapping are illegal activities in Brazil (Brasil 1967), flight, Steven et al. 2011), which may ultimately affect therefore urban birds could have been associating humans' approximation as a non-threatening behavior (e.g. individual fitness and population survival. Therefore, we highlight that to improve the chances of native urban- Blumstein 2006, Weston et al. 2012, Guay et al. 2013), inhabitant bird species conservation it is important to ultimately leading to steady foraging rate. Furthermore, ensure that parks have human-free areas, in which birds the reduction on their adverse reactions to humans may could find refuge for foraging and resting especially in result from a foraging strategy optimized for ensuring days when the density of visitors increases such as during proper spatial and temporal exploration of resources weekends. in human populated habitats. When high number of humans occupy the parks, foraging may be hampered by the restricted amount of unoccupied foraging areas. To ACKNOWLEDGEMENTS overcome this problem, our data suggest that urban birds maximize their foraging efforts b y keep searching for food Authors thank a grant by CNPq to L.T.M. (455908/2014- despite of increased human proximity. 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Journal

Ornithology Research – Springer Journals

Published: Jun 1, 2018

Keywords: approaching experimental trial; escaping strategy; flight initiation distance; foraging rate; human density

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