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Leukocyte profiles and body condition of free-living Burrowing Owls (Athene cunicularia) from rural and urban areas in the Argentinean Pampas

Leukocyte profiles and body condition of free-living Burrowing Owls (Athene cunicularia) from... Revista Brasileira de Ornitologia 26(1): 45–51. ARTICLE March 2018 Leukocyte profiles and body condition of free-living Burrowing Owls (Athene cunicularia) from rural and urban areas in the Argentinean Pampas 1,3 1 1 2 1 Matilde Cavalli , Alejandro V. Baladrón , Juan P. Isacch , Verónica D'Amico & María S. Bó Grupo Vertebrados, Instituto de Investigaciones Marinas y Costeras (IIMyC), CONICET - Universidad Nacional de Mar del Plata, Funes 3350, Mar del Plata (B7602AYJ), Buenos Aires, Argentina. Centro Nacional Patagónico (CONICET), Boulevard Brown 2915, Puerto Madryn (U9120ACF), Chubut, Argentina. Corresponding author: mcavalli@mdp.edu.ar Received on 27 October 2017. Accepted on 06 March 2018. ABSTRACT: Animals living in urban areas are exposed to novel and potentially stressful human disturbances. In response to the increased number of stressors in these habitats, they may manifest changes in their immune system, body condition and physiology. Many bird species are negatively impacted by urbanization, whilst other species thrive in urban areas. The capacity to adjust the physiological responses to the stressors associated with urban areas may play a key role in explaining the success of some bird species in these environments. In this study, we compared indicators of physiological stress response and body condition in free- living Burrowing Owls (Athene cunicularia) inhabiting urban and rural areas. We calculated a scaled index of body condition, and assessed leukocyte profiles and t he heterophil/lymphocyte ratios of chicks and adults. We found no significant differences in these parameters between individuals from rural and urban areas. Chicks showed higher relative leukocyte counts than adults, which may be associated with ontogenetic development and immune system activation processes. KEY-WORDS: heterophil, leukocyte, lymphocyte, stress, urbanization. INTRODUCTION in maintaining stability may occur (Wada 2015). Two classes of hormones are involved in the With natural areas rapidly decreasing as human-altered modulation of physiological responses to stressors in habitats increase and human populations grow, bird vertebrates: catecholamines and glucocorticoids. The first involve t he release of noradrenaline and adrenaline species are finding themselves living ever closer to human habitats (Marzluff 2001). Some species have managed to from the sympathetic nervous system and the adrenal co-exist with humans in urban areas while others failed to medulla within seconds after detection of stressors, thrive in these new environments. Considering the rapid resulting in rapid physiological responses (Wada 2015). environmental change that occurs during urbanization, it On the other hand, glucocorticoids are secreted through the hypothalamic-pituitary-adrenal axis and are mainly may be predicted that only individuals capable of coping with challenges of urban life would succeed (Shanahan involved in recovery from stressors or preparing from et al. 2014). Species living in urban habitats are exposed future stressors. Glucocorticoids are secreted from adrenal to many novel and potentially stressful anthropogenic cortex within minutes after detecting a stressor and acts disturbances, such as permanent presence of humans, redirecting energy and behavior to essential adjustments (Wada 2015). The release of glucocorticoid hormones higher densities of non-native predators (e.g., cats and dogs), noise and light pollution as well as traffic (Sol et after a stressor is one of the mechanisms involved in al. 2013). Such urban challenges are predicted to trigger physiological coping mechanisms to long-term stress physiological and behavioural reactions that ultimately and, in vertebrates, is one of the mechanisms that ensure increase the levels of stress responses (Partecke et al. 2006, survival under adverse environmental conditions (Bonier 2012). However, prolonged or frequent stress responses Bonier et al. 2007, Bonier 2012, Johnstone et al. 2012). However, it is to be expected that if individuals are able can result in an individual entering a disease-like state of to cope with different levels of urban disturbance, then chronic stress leading to reduced fecundity and reduced living in urban contexts should not be perceived as more chances of survival (Siegel 1980, Wingfield & Sapolsky stressful than living in rural ones since a process involved 2003). Leukocyte profiles of wild Burrowing Owls Cavalli et al. Measuring chronic physiological stress in free- survive and prosper in urban habitats, often reaching living vertebrates can be problematic since reliable higher densities in such heavily disturbed habitats than in measurements of baseline levels of glucocorticoids are their natural habitats (Martínez et al. 2017). Living in close often difficult to obtain in the field because their levels proximity to humans presupposes a frequent exposure to rise immediately after capture (Davis 2005, Romero & anthropogenic stress factors, which Burrowing Owls have Reed 2005). The use of haematological parameters such overcome mainly through behavioral plasticity (Cavalli et as relative leukocyte (or white blood cell) counts made al. 2016a, 2016b). from blood smears represents an alternative method for The aim of this study was to compare leukocyte profile, measuring stress in birds since their values are related to the heterophil/lymphocyte ratio and body condition of levels of glucocorticoids hormones such as corticosterone, Burrowing Owls inhabiting urban and rural habitats of the avian stress hormone (Davis et al. 2008). A prolonged southeastern Pampas region. Considering that Burrowing increase of corticosterone levels in birds causes changes in Owls showed no breeding and behavioural limitations to the relative numbers of various specific leukocyte types establish in urban habitats (Cavalli et al. 2016a, 2016b, present within the immune system. For example, in Martínez et al. 2017) and have demonstrated a good ability response to corticosterone, circulating lymphocytes adhere to live in a wide variety of habitat types and with different to the endothelial cells and subsequently a significant levels of disturbance (Baladrón et al. 2016, Martínez et reduction in their circulating numbers is evidenced (Davis al. 2017), we hypothesize that this species presents good et al. 2008). Also, corticosterone stimulates an influx of adaptability to live in urban areas and should not perceive heterophils (the avian equivalent of the mammalian urban habitats as more stressful than rural areas. neutrophils) into the blood from the bone marrow and attenuates the egress of heterophils from the blood to METHODS other compartments (see Davis et al. 2008). Given the effect of stress hormones on leukocytes, leukocyte profiles and t he heterophil/lymphocyte The stud y was conducted in the southeast portion ratio have been widely used as indicators of response of the Pampas region of Argentina. The area was of individuals to several stressors such as temperature, dominated in the past by sand dunes, wetlands and grasslands (Vervoost 1967), and is nowadays a mosaic muscular exhaustion, food or water deprivation, captivity and contaminants among others (Siegel & Gross 2000, of different land-uses where agroecosystems (grazing Davis et al. 2008). Even though relative leukocyte ratios fields, croplands, and pasturelands) and thriving urban have been widely used as an estimator of long-term centers share the landscape (Pedrana et al. 2008). Here, stress or baseline hormones levels (Davis et al. 2008), Burrowing Owls inhabit rural habitats, vegetated sand dunes, and urban habitats (Baladrón et al. 2016). Urban some studies have shown that in some avian species the handling stress can significantly affect leukocyte counts and rural habitats were sampled in Mar Chiquita district o o within 30 and 60 min after capture (Cirule et al. 2012), (37 44.6'S; 57 25.7'W) and General Pueyrredón o o showing that leukocyte response to stress may be quicker district (38 00.8'S; 57 33.1'W). In these regions, urban than traditionally assumed. For this reason, the interval habitat is mostly represented by peri-urban areas (small touristic villages with < 800 inhabitants and scattered between bird capture and sample collection should be minimized to obtain a more precise estimation of baseline houses) and, to a lesser extent, suburban areas of larger cities (Pedrana et al. 2008, Zelaya et al. 2016). Rural stress level. Also, Müller et al. (2011) found in free-living kestrel nestlings that baseline corticosterone levels and habitats are mostly devoted to livestock production, the heterophil/lymphocyte ratio differ in the sensitivity thus grazing fields are th e dominant landscape unit, to various stressors suggesting that both measures should whereas croplands are limited to best-quality upland be taken when possible. soils. In this context, we defined urban habitats as built- up areas where owls will regularly encounter humans The Burrowing Owl (Athene cunicularia) is a ground-nesting raptor widely distributed throughout and considered as urban owls those whose nests were the mid to low latitude regions of Americas. Burrowing surrounded by more than 35 houses within a radius Owls' habitat has experienced important changes in the of 200 m. Rural habitat comprised open farmlands, last decades due to human activities, such as agriculture, grazing fields, and croplands, and distance from owl nests to houses in rural habitats was always greater than tourism and urbanization. It has been reported that some Burrowing Owl populations have been strongly 1 km. affected by habitat change in its northern range, to the Adults and chicks (~10 days old) from different point of being considered as threatened in some areas of nests were sampled during January 2014 and 2015. North America (Poulin et al. 2011). In contrast, at its Burrowing Owls were captured with noose carpets (Bloom et al. 2007). Two researchers remain constantly southernmost distribution this species has managed to Revista Brasileira de Ornitologia 26(1): 2018 Leukocyte profiles of wild Burrowing Owls Cavalli et al. watching traps with binoculars from a blind and run to The scaling exponent bSMA was calculated handle owls immediately after they were trapped. Owls were indirectly by dividing the slope from an ordinary least weighed using a spring scale (d = 5 g, precision ± 0.3%). squares regression on log transformed tarsus length A preliminary inspection of each captured individual was and body mass variables by the Pearson's correlation performed in order to register health status. Health status coefficient (r). We chose tarsus length as the proxy for of each individual was classified as healthy (i.e., no external skeletal body size as this measure has been routinely taken signs of illness based on the brightness of plumage, good during all captures. flight capacity in adults owls, absence of feather damage Leukocyte values were compared between owls from ectoparasites, and standard body mass: 198.5 ± 22.8 g from rural and urban habitats (only for adult owls since for adults, Baladrón et al. 2015) or non-healthy (i.e., missing no chicks were captured at rural habitats) and between feathers, presence of ectoparasites, below normal body mass), age groups (chicks and adults) using Student's t-test and and only those of the former group were used for further the nonparametric Mann-Whitney test when data did analyses. A drop of blood was extracted from their brachial not show a normal distribution. Normality was assessed vein using 0.5 mm needles. Samples were collected within by performing Shapiro-Wilk's test (Zar 2010). RLC 5 min of capture to minimize capture and handling stress was compared between habitats (rural and urban adult (Davis 2005). After collecting a blood sample and taking owls) and between age groups (chicks and adults) using morphometric measurements, we released owls at the same Mann-Whitney test. Scaled mass index of body condition place that they were captured. For all these procedures, we were compared between rural and urban adult owls by adhered to guidelines for the use of animals in research and Student's t-test (Zar 2010). A part of the data used to to the legal requirements of Argentina (permit numbers: calculate body condition belonged to a previous data set 2145-14331 and 22500-24871). that was partly published by Baladrón et al. (2015), but Thin smears from fresh blood were prepared none of the blood smears examined in this study were on individual slides, air dried, fixed with methanol obtained from owls examined in that study. (Reagents, Inc.) for 10 min and then stained with May-Grünwald (BIOPUR®) and Giemsa (BIOPUR®). Smears were examined using a light microscope scanning RESULTS monolayer fields with similar densities of erythrocytes for all individuals (Campbell 1994). The proportion Relative leukocyte counts, H/L ratios and RLC showed of each leukocyte type was obtained from a sample of no signific ant differenc es between rural and urban 100 leukocytes viewed in 1000× magnification (oil adult Burrowing Owls (P > 0.05, see Table 1). No immersion) and expressed as percentage of basophils signific ant differenc e was found between adult rural (B%), heterophils (H%), eosinophils (E%), lymphocytes and urban Burrowing Owls in scaled mass index of (L%), and monocytes (M%) (Campbell 1994). The body condition (mean urban owls = 205.5 g, SE = 3.8, heterophil/lymphocyte ratio (H/L) was calculated from n = 42; mean rural owls = 204.1 g, SE = 11.1, n = 9; the leukocyte counts and was used as an indicator of stress t = 0.15, df = 49, P = 0.88). Only one adult owl from (Davis et al. 2008). In general, higher H/L ratio values a rural habitat was excluded from our data set since indicate higher levels of individual stress while lower values it was classified as a non-healthy individual (missing indicate the opposite. Relative leukocyte count (RLC) feathers, body mass below the population mean: scaled per 10,000 erythrocytes was estimated by counting the mass index of body condition 149.7 g, had only one number of all erythrocytes in one microscopic visual field eye while the other showed infection signs evidenced and multiplied by the number of the microscopic visual by its color). fields that were scanned until rea ching 100 leukocytes, No signific ant differenc es were identified between following Lobato et al. (2005). age groups in heterophils (H), monocytes (M), basophiles Body mass (g) and tarsus length (mm, measured (B) and relative leukocyte counts (RLC) (P > 0.05, see with a digital caliper) was measured to calculate a body Table 2). Percentage of lymphocytes (L) was higher for condition index (Peig & Green 2009). Since both chicks than for adult Burrowing Owls while percentage variables do not differ between Burrowing Owls sexes of eosinophils (E) was higher for adults (Table 2). The (see Baladrón et al. 2015) we pooled them indistinctly. To H/L ratio was higher for adult than for chick Burrowing quantify body mass in relation to body size, we calculated Owls. Fig. 1 shows the morphology of erythrocytes, a scaled mass index of body condition following the heterophils, eosinophils, lymphocytes, monocytes and procedure described by Peig & Green (2009). The index thrombocytes. was calculated as follows: Average tarsus length of the study population Body mass of individual i × ( ) bSMA Individual tarsus length of individual i Revista Brasileira de Ornitologia 26(1): 2018 Leukocyte profiles of wild Burrowing Owls Cavalli et al. Figure 1. Burrowing Owl (Athene cunicularia) blood smears. Erythrocytes (Er), thrombocytes (T), heterophils (H), lymphocytes (L), eosinophils (E) and monocytes (M). × 100 objective. Table 1. Mean ± standard error (SE), range (minimum – maximum) of relative leukocyte counts, relative leukocyte count (RLC) and heterophil/lymphocyte ratio (H/L) from rural and urban adult Burrowing Owls (Athene cunicularia) from southeast of Pampas region in Argentina. Sample size (n) is shown in parentheses. Leukocyte types are expressed as percentage of heterophils (H%), lymphocytes (L%), monocytes (M%), basophils (B%) and eosinophils (E%). Rural (n = 4) Urban (n = 11) Statistical test P-values Mean ± SE Range Mean ± SE Range H% 36.1 ± 0.4 33.6 – 37.1 37.5 ± 3.6 19.0 – 61.4 t = - 0.2 0.81 L% 40.3 ± 0.7 38.9 – 42.0 35.7 ± 1.9 25.8 – 47.6 t = 1.3 0.13 M% 1.0 ± 0.7 0.88 – 3.1 0.9 ± 0.3 0.75 – 3.3 U = 21 0.94 B% 0.2 ± 0.2 0.0 – 0.7 0.1 ± 0.1 0.0 – 1.7 U = 19 0.58 E% 22.3 ± 1.9 18.1 – 27.2 25.5 ± 2.6 15.3 – 37.1 U = 27 0.55 H/L 0.9 ± 0.02 0.8 – 0.9 1.1 ± 0.1 0.4 – 1.5 U = 29 0.39 RLC 94.5 ± 25.2 121.0 – 160.0 91.0 ± 9.5 59.0 – 132.0 U = 23.5 1.00 Table 2. Mean ± standard error (SE), range (minimum – maximum) of relative leukocyte counts, relative leukocyte count (RLC) and heterophil/lymphocyte ratio (H/L) from chick and adult Burrowing Owls (Athene cunicularia) from southeast of Pampas region in Argentina. Sample size (n) is shown in parentheses. Leukocyte types are expressed as percentage of heterophils (H%), lymphocytes (L%), monocytes (M%), basophils (B%) and eosinophils (E%). Chicks (n = 10) Adults (n = 15) Statistical test P-values Mean ± SE Range Mean ± SE Range H% 34.3 ± 2.2 27.3 – 46.4 37.2 ± 2.5 19.0 – 61.4 U = 91 0.36 L% 51.9 ± 2.3 39.5 – 63.0 36.9 ± 1.5 25.8 – 47.6 t = -5.6 <0.001 M% 0.5 ± 0.2 0.0 – 1.4 0.9 ± 0.3 0.0 – 3.3 U = 82 0.69 B% 0.0 ± 0.0 0.0 – 0.0 0.2 ± 0.1 0.0 – 1.6 U = 85 0.26 E% 13.3 ± 2.3 6.0 – 27.2 24.7 ± 1.9 12.9 – 37.1 t = 3.7 0.001 H/L 0.6 ± 0.1 0.5 – 1.0 1.1 ± 0.1 0.4 – 2.4 U = 120 0.01 RLC 76.6 ± 7.1 48.0 – 127.0 92.0 ± 9.3 39.0 – 160.0 U = 96.5 0.24 Revista Brasileira de Ornitologia 26(1): 2018 Leukocyte profiles of wild Burrowing Owls Cavalli et al. rural owls. Rebolo-Ifrán et al. (2015) recently reported DISCUSSION that feathers from urban and rural Burrowing Owls showed similar values of corticosterone, suggesting that Animals often respond to the challenges found in life in urban settings might not represent an additional urban areas through changes in their body condition source of stress for individuals living in this environment. and physiological stress responses (Davis et al. 2008). The per centage of eosinophils we observed in The magnitude and prevalence of stress levels may vary circulating blood was similar between owls from rural and according to the species and its tolerance to the different urban habitats and, in both habitats, values were higher stressor agents associated to urban life (i.e., if it is an than the typical reported for birds in general (e.g., E% = avoider, adaptable or exploiter of urban areas; Blair 2.5 – 5.6; Davis et al. 2008). This type of cell is strongly 1996, McKinney 2002). Our results show that leukocyte associated with helminth parasite load and activity profiles and t he body condition of wild Burrowing Owls (Johnstone et al. 2012). However, the high counts of did not differ significantly between urban and rural eosinophils observed for Burrowing Owls in our study is habitats, corroborating the notion that this is an urban- consistent with numbers reported for most healthy raptor adaptable species. This finding is similar to that reported species studied to date (Copete-Sierra 2013). In addition, for other urban-exploiter such as House Sparrows (Passer the low percentages of other leukocyte types, such as domesticus). Urban and rural House Sparrows have been monocytes (associated with defense against infections and show to display similar levels of stress hormones (Bókony bacteria) and basophils (associated with inflammatory et al. 2012) and their immunological status does not processes) (Campbell 1994), support the idea that the vary among urbanization levels (Chávez-Zichinelli et al. Burrowing Owls examined in this study were healthy. 2010). However, the range of indicators of physiological We found that chicks and adult Burrowing Owls stress response (immunoglobulin and corticosterone showed differences in relative leukocyte counts, which concentrations) is wider in habitats with more stressful could be explained by different developmental stages stimuli. In line with this idea, we found that urban areas of the immune system in young Burrowing Owls. The housed both high- and low-stressed owls, as relative thymus and bursa are proportionally up to 10 times larger counts for all leukocyte types showed wider ranges in in chicks than in adults, and lymphocytes are naturally urban areas in comparison to rural areas. more abundant in earlier stages of development (Maxwell In addition, we found that the heterophil-lymphocyte & Robertson 1998). As chicks grow, the number of (H/L) ratio, a parameter widely used as indicators of lymphocyte cells decrease and the thymus and bursa stress response, does not differ between urban and rural decrease in size (Maxwell & Robertson 1998, Dunbar et Burrowing Owls. This is similar to the pattern reported al. 2005). For these reasons, even though the H/L ratio has by Fokidis et al. (2008) for the Northern Mockingbird been considered a reliable index to determine individual (Mimus polyglottos), which is also an urban-adaptable physiological condition and a stress indicator (Maxwell species. However, these authors also reported the same & Robertson 1998, Davis et al. 2008), the differences for the Curve-billed Thrasher (Toxostoma curvirostre), observed in Burrowing Owls' H/L ratio between ages an urban avoider species. This suggests that the ability is probably related to the ontogenetic development to cope with human stressors in urban habitats might be rather than to a difference in how t hey respond to stress associated with intrinsic characteristics of each species situations. and with its capacity to adapt to new environmental In summary, our study indicates that urban conditions, or alternately it could be interpreted as Burrowing Owls show similar relative leukocyte counts, indicating that the physiological responses to urban H/L ratios, and body condition than rural individuals. stressors might not necessarily involve substantial changes Even when such similarity may be influenced by the to the H/L ratio. analytical tool employed (e.g., another parameter Even though leukocyte counts and the H/L ratio are different of H/L ratio and RLC should have been used) considered reliable stress indicators in birds (Davis et al. or the limited sample (e.g., a relatively small number of 2008), some authors argue that these variables should be rural individuals was sampled), our findings suggest that interpreted cautiously since they may vary in response to living in urban habitats might not significantly affect the inflammatory or infectious processes. In this sense, it has haematological parameters of Burrowing Owls. been suggested that the H/L ratio should be considered a complementary measure to the corticosterone level in blood and that these parameters are not interchangeable ACKNOWLEDGEMENTS (Müller et al. 2011). Regarding this, it would be interesting to incorporate corticosterone level information into future We thank N. Martínez-Curci, L. Biondi, R. Zenuto and studies comparing physiological stress between urban and F. Vera for their help and suggestions during previous Revista Brasileira de Ornitologia 26(1): 2018 Leukocyte profiles of wild Burrowing Owls Cavalli et al. Functional Ecology 22: 760–772. stages of this work. We thank Grupo Invertebrados Dunbar M.R., Greg M.A., Crawfordd J.A., Giordano M.R. & from UNMdP for lending the microscope camera. We Tornquist S.J. 2005. 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Leukocyte profiles and body condition of free-living Burrowing Owls (Athene cunicularia) from rural and urban areas in the Argentinean Pampas

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2178-7875
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10.1007/bf03544414
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Revista Brasileira de Ornitologia 26(1): 45–51. ARTICLE March 2018 Leukocyte profiles and body condition of free-living Burrowing Owls (Athene cunicularia) from rural and urban areas in the Argentinean Pampas 1,3 1 1 2 1 Matilde Cavalli , Alejandro V. Baladrón , Juan P. Isacch , Verónica D'Amico & María S. Bó Grupo Vertebrados, Instituto de Investigaciones Marinas y Costeras (IIMyC), CONICET - Universidad Nacional de Mar del Plata, Funes 3350, Mar del Plata (B7602AYJ), Buenos Aires, Argentina. Centro Nacional Patagónico (CONICET), Boulevard Brown 2915, Puerto Madryn (U9120ACF), Chubut, Argentina. Corresponding author: mcavalli@mdp.edu.ar Received on 27 October 2017. Accepted on 06 March 2018. ABSTRACT: Animals living in urban areas are exposed to novel and potentially stressful human disturbances. In response to the increased number of stressors in these habitats, they may manifest changes in their immune system, body condition and physiology. Many bird species are negatively impacted by urbanization, whilst other species thrive in urban areas. The capacity to adjust the physiological responses to the stressors associated with urban areas may play a key role in explaining the success of some bird species in these environments. In this study, we compared indicators of physiological stress response and body condition in free- living Burrowing Owls (Athene cunicularia) inhabiting urban and rural areas. We calculated a scaled index of body condition, and assessed leukocyte profiles and t he heterophil/lymphocyte ratios of chicks and adults. We found no significant differences in these parameters between individuals from rural and urban areas. Chicks showed higher relative leukocyte counts than adults, which may be associated with ontogenetic development and immune system activation processes. KEY-WORDS: heterophil, leukocyte, lymphocyte, stress, urbanization. INTRODUCTION in maintaining stability may occur (Wada 2015). Two classes of hormones are involved in the With natural areas rapidly decreasing as human-altered modulation of physiological responses to stressors in habitats increase and human populations grow, bird vertebrates: catecholamines and glucocorticoids. The first involve t he release of noradrenaline and adrenaline species are finding themselves living ever closer to human habitats (Marzluff 2001). Some species have managed to from the sympathetic nervous system and the adrenal co-exist with humans in urban areas while others failed to medulla within seconds after detection of stressors, thrive in these new environments. Considering the rapid resulting in rapid physiological responses (Wada 2015). environmental change that occurs during urbanization, it On the other hand, glucocorticoids are secreted through the hypothalamic-pituitary-adrenal axis and are mainly may be predicted that only individuals capable of coping with challenges of urban life would succeed (Shanahan involved in recovery from stressors or preparing from et al. 2014). Species living in urban habitats are exposed future stressors. Glucocorticoids are secreted from adrenal to many novel and potentially stressful anthropogenic cortex within minutes after detecting a stressor and acts disturbances, such as permanent presence of humans, redirecting energy and behavior to essential adjustments (Wada 2015). The release of glucocorticoid hormones higher densities of non-native predators (e.g., cats and dogs), noise and light pollution as well as traffic (Sol et after a stressor is one of the mechanisms involved in al. 2013). Such urban challenges are predicted to trigger physiological coping mechanisms to long-term stress physiological and behavioural reactions that ultimately and, in vertebrates, is one of the mechanisms that ensure increase the levels of stress responses (Partecke et al. 2006, survival under adverse environmental conditions (Bonier 2012). However, prolonged or frequent stress responses Bonier et al. 2007, Bonier 2012, Johnstone et al. 2012). However, it is to be expected that if individuals are able can result in an individual entering a disease-like state of to cope with different levels of urban disturbance, then chronic stress leading to reduced fecundity and reduced living in urban contexts should not be perceived as more chances of survival (Siegel 1980, Wingfield & Sapolsky stressful than living in rural ones since a process involved 2003). Leukocyte profiles of wild Burrowing Owls Cavalli et al. Measuring chronic physiological stress in free- survive and prosper in urban habitats, often reaching living vertebrates can be problematic since reliable higher densities in such heavily disturbed habitats than in measurements of baseline levels of glucocorticoids are their natural habitats (Martínez et al. 2017). Living in close often difficult to obtain in the field because their levels proximity to humans presupposes a frequent exposure to rise immediately after capture (Davis 2005, Romero & anthropogenic stress factors, which Burrowing Owls have Reed 2005). The use of haematological parameters such overcome mainly through behavioral plasticity (Cavalli et as relative leukocyte (or white blood cell) counts made al. 2016a, 2016b). from blood smears represents an alternative method for The aim of this study was to compare leukocyte profile, measuring stress in birds since their values are related to the heterophil/lymphocyte ratio and body condition of levels of glucocorticoids hormones such as corticosterone, Burrowing Owls inhabiting urban and rural habitats of the avian stress hormone (Davis et al. 2008). A prolonged southeastern Pampas region. Considering that Burrowing increase of corticosterone levels in birds causes changes in Owls showed no breeding and behavioural limitations to the relative numbers of various specific leukocyte types establish in urban habitats (Cavalli et al. 2016a, 2016b, present within the immune system. For example, in Martínez et al. 2017) and have demonstrated a good ability response to corticosterone, circulating lymphocytes adhere to live in a wide variety of habitat types and with different to the endothelial cells and subsequently a significant levels of disturbance (Baladrón et al. 2016, Martínez et reduction in their circulating numbers is evidenced (Davis al. 2017), we hypothesize that this species presents good et al. 2008). Also, corticosterone stimulates an influx of adaptability to live in urban areas and should not perceive heterophils (the avian equivalent of the mammalian urban habitats as more stressful than rural areas. neutrophils) into the blood from the bone marrow and attenuates the egress of heterophils from the blood to METHODS other compartments (see Davis et al. 2008). Given the effect of stress hormones on leukocytes, leukocyte profiles and t he heterophil/lymphocyte The stud y was conducted in the southeast portion ratio have been widely used as indicators of response of the Pampas region of Argentina. The area was of individuals to several stressors such as temperature, dominated in the past by sand dunes, wetlands and grasslands (Vervoost 1967), and is nowadays a mosaic muscular exhaustion, food or water deprivation, captivity and contaminants among others (Siegel & Gross 2000, of different land-uses where agroecosystems (grazing Davis et al. 2008). Even though relative leukocyte ratios fields, croplands, and pasturelands) and thriving urban have been widely used as an estimator of long-term centers share the landscape (Pedrana et al. 2008). Here, stress or baseline hormones levels (Davis et al. 2008), Burrowing Owls inhabit rural habitats, vegetated sand dunes, and urban habitats (Baladrón et al. 2016). Urban some studies have shown that in some avian species the handling stress can significantly affect leukocyte counts and rural habitats were sampled in Mar Chiquita district o o within 30 and 60 min after capture (Cirule et al. 2012), (37 44.6'S; 57 25.7'W) and General Pueyrredón o o showing that leukocyte response to stress may be quicker district (38 00.8'S; 57 33.1'W). In these regions, urban than traditionally assumed. For this reason, the interval habitat is mostly represented by peri-urban areas (small touristic villages with < 800 inhabitants and scattered between bird capture and sample collection should be minimized to obtain a more precise estimation of baseline houses) and, to a lesser extent, suburban areas of larger cities (Pedrana et al. 2008, Zelaya et al. 2016). Rural stress level. Also, Müller et al. (2011) found in free-living kestrel nestlings that baseline corticosterone levels and habitats are mostly devoted to livestock production, the heterophil/lymphocyte ratio differ in the sensitivity thus grazing fields are th e dominant landscape unit, to various stressors suggesting that both measures should whereas croplands are limited to best-quality upland be taken when possible. soils. In this context, we defined urban habitats as built- up areas where owls will regularly encounter humans The Burrowing Owl (Athene cunicularia) is a ground-nesting raptor widely distributed throughout and considered as urban owls those whose nests were the mid to low latitude regions of Americas. Burrowing surrounded by more than 35 houses within a radius Owls' habitat has experienced important changes in the of 200 m. Rural habitat comprised open farmlands, last decades due to human activities, such as agriculture, grazing fields, and croplands, and distance from owl nests to houses in rural habitats was always greater than tourism and urbanization. It has been reported that some Burrowing Owl populations have been strongly 1 km. affected by habitat change in its northern range, to the Adults and chicks (~10 days old) from different point of being considered as threatened in some areas of nests were sampled during January 2014 and 2015. North America (Poulin et al. 2011). In contrast, at its Burrowing Owls were captured with noose carpets (Bloom et al. 2007). Two researchers remain constantly southernmost distribution this species has managed to Revista Brasileira de Ornitologia 26(1): 2018 Leukocyte profiles of wild Burrowing Owls Cavalli et al. watching traps with binoculars from a blind and run to The scaling exponent bSMA was calculated handle owls immediately after they were trapped. Owls were indirectly by dividing the slope from an ordinary least weighed using a spring scale (d = 5 g, precision ± 0.3%). squares regression on log transformed tarsus length A preliminary inspection of each captured individual was and body mass variables by the Pearson's correlation performed in order to register health status. Health status coefficient (r). We chose tarsus length as the proxy for of each individual was classified as healthy (i.e., no external skeletal body size as this measure has been routinely taken signs of illness based on the brightness of plumage, good during all captures. flight capacity in adults owls, absence of feather damage Leukocyte values were compared between owls from ectoparasites, and standard body mass: 198.5 ± 22.8 g from rural and urban habitats (only for adult owls since for adults, Baladrón et al. 2015) or non-healthy (i.e., missing no chicks were captured at rural habitats) and between feathers, presence of ectoparasites, below normal body mass), age groups (chicks and adults) using Student's t-test and and only those of the former group were used for further the nonparametric Mann-Whitney test when data did analyses. A drop of blood was extracted from their brachial not show a normal distribution. Normality was assessed vein using 0.5 mm needles. Samples were collected within by performing Shapiro-Wilk's test (Zar 2010). RLC 5 min of capture to minimize capture and handling stress was compared between habitats (rural and urban adult (Davis 2005). After collecting a blood sample and taking owls) and between age groups (chicks and adults) using morphometric measurements, we released owls at the same Mann-Whitney test. Scaled mass index of body condition place that they were captured. For all these procedures, we were compared between rural and urban adult owls by adhered to guidelines for the use of animals in research and Student's t-test (Zar 2010). A part of the data used to to the legal requirements of Argentina (permit numbers: calculate body condition belonged to a previous data set 2145-14331 and 22500-24871). that was partly published by Baladrón et al. (2015), but Thin smears from fresh blood were prepared none of the blood smears examined in this study were on individual slides, air dried, fixed with methanol obtained from owls examined in that study. (Reagents, Inc.) for 10 min and then stained with May-Grünwald (BIOPUR®) and Giemsa (BIOPUR®). Smears were examined using a light microscope scanning RESULTS monolayer fields with similar densities of erythrocytes for all individuals (Campbell 1994). The proportion Relative leukocyte counts, H/L ratios and RLC showed of each leukocyte type was obtained from a sample of no signific ant differenc es between rural and urban 100 leukocytes viewed in 1000× magnification (oil adult Burrowing Owls (P > 0.05, see Table 1). No immersion) and expressed as percentage of basophils signific ant differenc e was found between adult rural (B%), heterophils (H%), eosinophils (E%), lymphocytes and urban Burrowing Owls in scaled mass index of (L%), and monocytes (M%) (Campbell 1994). The body condition (mean urban owls = 205.5 g, SE = 3.8, heterophil/lymphocyte ratio (H/L) was calculated from n = 42; mean rural owls = 204.1 g, SE = 11.1, n = 9; the leukocyte counts and was used as an indicator of stress t = 0.15, df = 49, P = 0.88). Only one adult owl from (Davis et al. 2008). In general, higher H/L ratio values a rural habitat was excluded from our data set since indicate higher levels of individual stress while lower values it was classified as a non-healthy individual (missing indicate the opposite. Relative leukocyte count (RLC) feathers, body mass below the population mean: scaled per 10,000 erythrocytes was estimated by counting the mass index of body condition 149.7 g, had only one number of all erythrocytes in one microscopic visual field eye while the other showed infection signs evidenced and multiplied by the number of the microscopic visual by its color). fields that were scanned until rea ching 100 leukocytes, No signific ant differenc es were identified between following Lobato et al. (2005). age groups in heterophils (H), monocytes (M), basophiles Body mass (g) and tarsus length (mm, measured (B) and relative leukocyte counts (RLC) (P > 0.05, see with a digital caliper) was measured to calculate a body Table 2). Percentage of lymphocytes (L) was higher for condition index (Peig & Green 2009). Since both chicks than for adult Burrowing Owls while percentage variables do not differ between Burrowing Owls sexes of eosinophils (E) was higher for adults (Table 2). The (see Baladrón et al. 2015) we pooled them indistinctly. To H/L ratio was higher for adult than for chick Burrowing quantify body mass in relation to body size, we calculated Owls. Fig. 1 shows the morphology of erythrocytes, a scaled mass index of body condition following the heterophils, eosinophils, lymphocytes, monocytes and procedure described by Peig & Green (2009). The index thrombocytes. was calculated as follows: Average tarsus length of the study population Body mass of individual i × ( ) bSMA Individual tarsus length of individual i Revista Brasileira de Ornitologia 26(1): 2018 Leukocyte profiles of wild Burrowing Owls Cavalli et al. Figure 1. Burrowing Owl (Athene cunicularia) blood smears. Erythrocytes (Er), thrombocytes (T), heterophils (H), lymphocytes (L), eosinophils (E) and monocytes (M). × 100 objective. Table 1. Mean ± standard error (SE), range (minimum – maximum) of relative leukocyte counts, relative leukocyte count (RLC) and heterophil/lymphocyte ratio (H/L) from rural and urban adult Burrowing Owls (Athene cunicularia) from southeast of Pampas region in Argentina. Sample size (n) is shown in parentheses. Leukocyte types are expressed as percentage of heterophils (H%), lymphocytes (L%), monocytes (M%), basophils (B%) and eosinophils (E%). Rural (n = 4) Urban (n = 11) Statistical test P-values Mean ± SE Range Mean ± SE Range H% 36.1 ± 0.4 33.6 – 37.1 37.5 ± 3.6 19.0 – 61.4 t = - 0.2 0.81 L% 40.3 ± 0.7 38.9 – 42.0 35.7 ± 1.9 25.8 – 47.6 t = 1.3 0.13 M% 1.0 ± 0.7 0.88 – 3.1 0.9 ± 0.3 0.75 – 3.3 U = 21 0.94 B% 0.2 ± 0.2 0.0 – 0.7 0.1 ± 0.1 0.0 – 1.7 U = 19 0.58 E% 22.3 ± 1.9 18.1 – 27.2 25.5 ± 2.6 15.3 – 37.1 U = 27 0.55 H/L 0.9 ± 0.02 0.8 – 0.9 1.1 ± 0.1 0.4 – 1.5 U = 29 0.39 RLC 94.5 ± 25.2 121.0 – 160.0 91.0 ± 9.5 59.0 – 132.0 U = 23.5 1.00 Table 2. Mean ± standard error (SE), range (minimum – maximum) of relative leukocyte counts, relative leukocyte count (RLC) and heterophil/lymphocyte ratio (H/L) from chick and adult Burrowing Owls (Athene cunicularia) from southeast of Pampas region in Argentina. Sample size (n) is shown in parentheses. Leukocyte types are expressed as percentage of heterophils (H%), lymphocytes (L%), monocytes (M%), basophils (B%) and eosinophils (E%). Chicks (n = 10) Adults (n = 15) Statistical test P-values Mean ± SE Range Mean ± SE Range H% 34.3 ± 2.2 27.3 – 46.4 37.2 ± 2.5 19.0 – 61.4 U = 91 0.36 L% 51.9 ± 2.3 39.5 – 63.0 36.9 ± 1.5 25.8 – 47.6 t = -5.6 <0.001 M% 0.5 ± 0.2 0.0 – 1.4 0.9 ± 0.3 0.0 – 3.3 U = 82 0.69 B% 0.0 ± 0.0 0.0 – 0.0 0.2 ± 0.1 0.0 – 1.6 U = 85 0.26 E% 13.3 ± 2.3 6.0 – 27.2 24.7 ± 1.9 12.9 – 37.1 t = 3.7 0.001 H/L 0.6 ± 0.1 0.5 – 1.0 1.1 ± 0.1 0.4 – 2.4 U = 120 0.01 RLC 76.6 ± 7.1 48.0 – 127.0 92.0 ± 9.3 39.0 – 160.0 U = 96.5 0.24 Revista Brasileira de Ornitologia 26(1): 2018 Leukocyte profiles of wild Burrowing Owls Cavalli et al. rural owls. Rebolo-Ifrán et al. (2015) recently reported DISCUSSION that feathers from urban and rural Burrowing Owls showed similar values of corticosterone, suggesting that Animals often respond to the challenges found in life in urban settings might not represent an additional urban areas through changes in their body condition source of stress for individuals living in this environment. and physiological stress responses (Davis et al. 2008). The per centage of eosinophils we observed in The magnitude and prevalence of stress levels may vary circulating blood was similar between owls from rural and according to the species and its tolerance to the different urban habitats and, in both habitats, values were higher stressor agents associated to urban life (i.e., if it is an than the typical reported for birds in general (e.g., E% = avoider, adaptable or exploiter of urban areas; Blair 2.5 – 5.6; Davis et al. 2008). This type of cell is strongly 1996, McKinney 2002). Our results show that leukocyte associated with helminth parasite load and activity profiles and t he body condition of wild Burrowing Owls (Johnstone et al. 2012). However, the high counts of did not differ significantly between urban and rural eosinophils observed for Burrowing Owls in our study is habitats, corroborating the notion that this is an urban- consistent with numbers reported for most healthy raptor adaptable species. This finding is similar to that reported species studied to date (Copete-Sierra 2013). In addition, for other urban-exploiter such as House Sparrows (Passer the low percentages of other leukocyte types, such as domesticus). Urban and rural House Sparrows have been monocytes (associated with defense against infections and show to display similar levels of stress hormones (Bókony bacteria) and basophils (associated with inflammatory et al. 2012) and their immunological status does not processes) (Campbell 1994), support the idea that the vary among urbanization levels (Chávez-Zichinelli et al. Burrowing Owls examined in this study were healthy. 2010). However, the range of indicators of physiological We found that chicks and adult Burrowing Owls stress response (immunoglobulin and corticosterone showed differences in relative leukocyte counts, which concentrations) is wider in habitats with more stressful could be explained by different developmental stages stimuli. In line with this idea, we found that urban areas of the immune system in young Burrowing Owls. The housed both high- and low-stressed owls, as relative thymus and bursa are proportionally up to 10 times larger counts for all leukocyte types showed wider ranges in in chicks than in adults, and lymphocytes are naturally urban areas in comparison to rural areas. more abundant in earlier stages of development (Maxwell In addition, we found that the heterophil-lymphocyte & Robertson 1998). As chicks grow, the number of (H/L) ratio, a parameter widely used as indicators of lymphocyte cells decrease and the thymus and bursa stress response, does not differ between urban and rural decrease in size (Maxwell & Robertson 1998, Dunbar et Burrowing Owls. This is similar to the pattern reported al. 2005). For these reasons, even though the H/L ratio has by Fokidis et al. (2008) for the Northern Mockingbird been considered a reliable index to determine individual (Mimus polyglottos), which is also an urban-adaptable physiological condition and a stress indicator (Maxwell species. However, these authors also reported the same & Robertson 1998, Davis et al. 2008), the differences for the Curve-billed Thrasher (Toxostoma curvirostre), observed in Burrowing Owls' H/L ratio between ages an urban avoider species. This suggests that the ability is probably related to the ontogenetic development to cope with human stressors in urban habitats might be rather than to a difference in how t hey respond to stress associated with intrinsic characteristics of each species situations. and with its capacity to adapt to new environmental In summary, our study indicates that urban conditions, or alternately it could be interpreted as Burrowing Owls show similar relative leukocyte counts, indicating that the physiological responses to urban H/L ratios, and body condition than rural individuals. stressors might not necessarily involve substantial changes Even when such similarity may be influenced by the to the H/L ratio. analytical tool employed (e.g., another parameter Even though leukocyte counts and the H/L ratio are different of H/L ratio and RLC should have been used) considered reliable stress indicators in birds (Davis et al. or the limited sample (e.g., a relatively small number of 2008), some authors argue that these variables should be rural individuals was sampled), our findings suggest that interpreted cautiously since they may vary in response to living in urban habitats might not significantly affect the inflammatory or infectious processes. In this sense, it has haematological parameters of Burrowing Owls. been suggested that the H/L ratio should be considered a complementary measure to the corticosterone level in blood and that these parameters are not interchangeable ACKNOWLEDGEMENTS (Müller et al. 2011). Regarding this, it would be interesting to incorporate corticosterone level information into future We thank N. Martínez-Curci, L. Biondi, R. Zenuto and studies comparing physiological stress between urban and F. Vera for their help and suggestions during previous Revista Brasileira de Ornitologia 26(1): 2018 Leukocyte profiles of wild Burrowing Owls Cavalli et al. Functional Ecology 22: 760–772. stages of this work. We thank Grupo Invertebrados Dunbar M.R., Greg M.A., Crawfordd J.A., Giordano M.R. & from UNMdP for lending the microscope camera. We Tornquist S.J. 2005. 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Revista Brasileira de Ornitologia 26(1): 2018

Journal

Ornithology ResearchSpringer Journals

Published: Mar 1, 2018

Keywords: heterophil; leukocyte; lymphocyte; stress; urbanization

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