Stability in Prey Abundance May Buffer Black Sparrowhawks Accipiter Melanoleucus from Health Impacts of Urbanization

Ibis (2016), 159,38–54

Stability in prey abundance may buffer Black Sparrowhawks Accipiter melanoleucus from health impacts of urbanization

JESSLEENA SURI,* PETRA SUMASGUTNER, EL EONORE HELLARD, ANN KOESLAG & ARJUN AMAR Department of Biological Sciences, Percy FitzPatrick Institute of African Ornithology, DST-NRF Centre of Excellence, University of Cape Town, Rondebosch, Cape Town 7701, South Africa

As the global trend towards urbanization continues, the need to understand its impact on wildlife grows. Species may have different levels of tolerance to urban disturbance; some even appear to thrive in urban areas and use human-subsidized resources. However, the physiological costs and trade-offs faced by urban-dwelling species are still poorly under- stood. We assess the evidence for a negative impact of urbanization on the Black Spar- rowhawk Accipiter melanoleucus, a raptor that recently colonized Cape Town, South Africa, and explore the potential mechanisms behind any such effect. We predicted that birds in more urbanized areas may be in poorer health and that this may be partially dri- ven by differences in prey quantity and quality along an urban habitat gradient. The health of Black Sparrowhawk nestlings was evaluated through measures of their physiological stress (heterophil/lymphocyte ratio), body condition and blood parasite infection (infection risk and intensity of Haemoproteus and Leucocytozoon). Diet composition was determined through an analysis of prey remains collected around nests, and prey abundance was determined through point counts in different habitat types. We could find no negative effects of urbanization on nestling health, with no significant relationships with heterophil/lymphocyte ratio, body condition, risk and intensity of infection by Haemopro- teus or intensity of infection by Leucocytozoon. Risk of infection by Leucocytozoon did, however, decline with increasing urban cover, perhaps because urbanized areas contain less habitat for blackflies, the vectors of this parasite, which require moving fresh water. We found no change in diet breadth or composition with increasing urban cover. Although some prey species were abundant or less abundant in certain habitat types, all habitat types contained ample prey for Black Sparrowhawks. The widespread abundance of food resources and resulting lack of nutritional stress may explain why Black Sparrowhawks are seemingly free of the negative health impacts expected to arise from urbanization. These findings may explain the success of the species in Cape Town and suggest that for urban- dwelling, bird-eating raptors the abundance of prey in cities may override any potential negative impacts of urbanization on health due to disturbance or other sources of stress. Keywords: body condition, diet, Leucocytozoon, Haemoproteus, heterophil/lymphocyte ratio, leucocyte profile, raptor, urban stress.

As natural areas are rapidly being transformed into 2011). Urbanization often results in the rearrange- cities and the majority of the world’s population ment of biotic assemblages, whereby natural habi- now live in urban areas, increasing emphasis is tats are replaced with human-dominated being placed on biological research and conserva- landscapes containing novel species compositions tion within cities (Grimm et al. 2008, Kowarik and interactions (McDonald et al. 2008, Ortega- Alvarez & MacGregor-Fors 2009). Urban ecologists have suggested that species can be divided *Corresponding author. Email: [email protected] into three groups based on their levels of tolerance

to urban disturbance – urban ‘avoiders’, ‘adapters’ interactions between hosts and pathogens. The and ‘exploiters’ (Blair 1999, McKinney 2002). increased densities and contact between humans, Urban exploiters are a group of mainly non-native domestic and wildlife species, and sometimes the species such as Feral Pigeons Columba livia or abundance of favourable environments for parasite Common Starlings Sturnus vulgaris, whose wide- vectors, can increase the transmission of infectious spread success in urban areas is related to their diseases or favour the (re)emergence of pathogens ability to exploit anthropogenic resources such as in urban environments (Ditchkoff et al. 2006, garbage dumps, feeders or nestboxes, on which Brearley et al. 2012). In addition, higher levels of they are largely dependent (McKinney 2002). physiological stress faced by animals in cities can Urban adapters make use of both natural resources compromise their immune ability and increase and those subsidized by humans, and are thus their susceptibility to pathogens (Bradley & Altizer more flexible in their lifestyles (McKinney 2002). 2007, Brearley et al. 2012, Giraudeau et al. 2014). Urban-avoiding species are those that are highly Urbanization can further alter interspecific interac- sensitive to stressors and have very specific tions by disrupting trophic interactions in complex resource requirements, and thus tend not to occur multi-species networks, changing distribution pat- in cities (McKinney 2002). Although such divi- terns of predators, prey and competitors or shifting sions are generally widely accepted, our mechanis- phenologies, producing trophic mismatches, sur- tic understanding of smaller-scale impacts on plus or shortages in food supply or imbalances in species’ ecology and physiology remains weaker nutritional quality of food (Shochat 2004, Fischer (Giraudeau et al. 2014, Almasi et al. 2015, Hahs et al. 2012, Isaksson 2015). An appreciation of & Evans 2015, Isaksson 2015). An apparently how these impacts interact is important for under- urban-exploiting or adapting species may be able standing the short- and long-term fitness of species to make use of abundant resources in the short in cities. term, but other costs of urban living may under- Raptors are particularly interesting to study in mine its long-term health and persistence in an an urban context. They are often considered apex urban environment. In this way, cities may act as predators and umbrella species and their loss can ecological traps – habitats that appear attractive have cascading effects on food webs (Palomino & due to abundant food or nest-sites, but are in fact Carrascal 2007, Lyly et al. 2015, Donazar et al. unsuitable due to novel threats, disturbance, dis- 2016, Mueller et al. 2016). Raptors can be vulner- ease or low food quality (Mannan & Boal 2004, able to a wide range of threats since their success Rutz 2006, 2008, Sumasgutner et al. 2014). is often dependent on relatively large tracts of There can be both positive and negative effects good habitat with a stable prey supply (Newton of urbanization and these effects may differ at the 1979, Amar et al. 2008). In urban areas, they individual, population and community levels may face additional threats due to direct persecu- (Almasi et al. 2015). Direct and indirect distur- tion and poisoning (Mannan & Boal 2004) or to bances in urban areas can include air pollution injuries arising from human infrastructure, such as (Kylin et al. 2011), noise (Slabbekoorn & Rip- collision with traffic, power lines and glass meester 2008, Moiron et al. 2015) or light pollu- (Donazar et al. 2016). In spite of this, the trend of tion (Gaston et al. 2015), diet (Shochat 2004, raptors colonizing cities is on the rise. More spe- Faeth et al. 2005, Andersson et al. 2015, Isaksson cies are moving into urbanized areas, for example 2015), changes in predation pressure (Fischer Crested Goshawk Accipiter trivirgatus (Lin et al. et al. 2012, Møller 2010, 2011, 2012), urban 2015), Crowned Eagle Stephanoaetus coronatus heat island effects (Kaiser et al. 2016), collision (McPherson et al. 2015, Reeves & Boshoff 2015) with cars and windows (Ortega-Alvarez & and, the focus of this study, Black Sparrowhawk MacGregor-Fors 2009), electrocution (Palomino & Accipiter melanoleucus (Martin et al. 2014b). Many Carrascal 2007) and predation by domestic ani- species of raptors are attracted to urban areas mals (Ditchkoff et al. 2006). These disturbances because of high concentrations of prey in relation can elicit responses at different levels, leading for to surrounding natural areas (Chace & Walsh instance to oxidative stress, altered immune 2006, Rutz 2008, Solonen & Ursin 2008, Donazar defences or changes in foraging behaviour (Ditch- et al. 2016). However, cities may also pose more koff et al. 2006, Almasi et al. 2015, Isaksson subtle physiological risks to raptors, which may 2015). Urbanization is also likely to alter result in maladaptive characteristics or reduce

long-term fitness. Examining the mechanisms conditions of physiological stress, illness or pollu- behind the perceived success of raptors in urban tion, the secretion of glucocorticoids leads to an areas can thus help to establish whether these spe- elevation in the number of heterophils in the cies are falling into ecological traps or whether blood and a decrease in the number of lympho- they are genuine urban-adapters. cytes, and thus an increase in the H/L ratio (Davis In this study we explore some of these ques- et al. 2008). Studies have shown that the H/L tions in the Black Sparrowhawk and determine ratio is indicative of environmental stressors (Mul- whether it may be suffering from hidden conse- ler et al. 2011) and human-induced habitat quences of urban living. In South Africa, the Black changes (Banbura et al. 2013). Blood parasite Sparrowhawk has experienced a rapid range infection was used to disentangle potential expansion south and westwards (Hockey & Midg- changes in host–parasite interactions along the ley 2009), which has brought them into contact urban gradient, with a focus on Haemoproteus nisi with urban landscapes (Sumasgutner et al. 2016c). and Leucocytozoon toddi, parasites known to circu- Their expansion has largely been attributed to the late within this population of Black Sparrowhawks spread of exotic trees such as pines, eucalyptus (Lei et al. 2013). If a bird’s immune system is and poplars in plantations, gardens and parks, compromised due to urbanization, the intensity of which have provided prime nesting sites (Malan & infections should increase with urban cover, and Robinson 1999, 2001). They may also benefit so should their infection risk (probability of infec- from the proliferation of their main prey, pigeons tion as estimated from the presence or absence of and doves (Columbidae), in urban areas (Malan & parasites in individuals sampled) if they are more Robinson 1999). Human-altered environments exposed to vectors (biting midges and simuliid may therefore provide resources that are central to flies, respectively; Valkiunas 2005) in more urban- the success of Black Sparrowhawks on the Cape ized areas. Peninsula (Malan & Robinson 1999, 2001). How- Finally, we investigated the diet composition, ever, whether exposure to urban environments diet breadth and abundance of the key prey spe- may also be having negative consequences on indi- cies along the urban gradient in order to assess the vidual birds is unknown. Addressing these ques- potential role of diet as a mechanism of health tions could help in predicting the impacts of alteration within urban habitats. For example, cer- urbanization on other similar species, while shed- tain urban-exploiting species such as pigeons might ding light on the mechanisms behind the success feature more prominently in the diet of urban of Black Sparrowhawks on the Cape Peninsula. Black Sparrowhawks, and feeding disproportion- Taking advantage of the long-term study of the ately on such species might translate into compro- Black Sparrowhawk population on the Cape mised health in Black Sparrowhawk nestlings due Peninsula (Martin et al. 2014a), we aimed to to the presence of pollutants and pathogens in determine the impacts of urbanization on the prey, or to their poor nutritional quality as a result health and diet of this species. We focused on of feeding on urban ‘junk food’ (Estes & Mannan body condition, leucocyte profiles and blood para- 2003, Shochat 2004, Isaksson 2015). Carotenoid site infection to determine the health status of levels in urban-dwelling prey species may be lower nestlings. Body condition is a measure of the fat due to the low-quality food resources on which content or nutrient reserves of an animal and can they forage, for example at bird feeders or rubbish be an indicator of chronic disturbance and nutri- dumps (Isaksson et al. 2005, Isaksson & Andersson tional stress (Labocha & Hayes 2012, Almasi et al. 2007, Isaksson 2009). This could have an impact 2015). Leucocyte profiles are also used as indica- because carotenoid rich-food sources can improve tors of immune condition and stress (Davis et al. individual health, particularly in the case of nest- 2008), as the relative frequencies of the leuco- lings (Sternalski et al. 2010, 2012a,b). Such effects cytes performing different functions fluctuate with of urbanization on diet quality can in turn alter an animal’s physiological condition. In particular, innate immune function, with negative impacts on the ratio of heterophils/lymphocytes (H/L ratio) fitness and survival (Hegemann et al. 2013, 2015). has been shown to be a reliable measure of physi- Alternatively, a lack of health impacts of urbaniza- ological stress, as it correlates with glucocorticoid tion might arise because urban habitats provide levels (i.e. stress hormones) without being sensi- prey of sufficient quantity and quality across differ- tive to handling time (Davis et al. 2008). Under ent levels of urbanization.

variation explained by sex (females are heavier METHODS than males) with ANOVA (following Roulin 2007). Data collection Diet estimation This study was undertaken on a resident breeding population of Black Sparrowhawks in Cape Town, Diet composition: prey remains analysis. We collected South Africa. The city is a mosaic of heavily urban- prey remains during monitoring visits between ized areas, suburbs, patches of indigenous Afromon- 2012 and 2015 underneath and around nest trees. tane forest and fynbos vegetation, wetlands and Bird-eating raptors such as Black Sparrowhawks artificial habitats such as gardens, golf courses, exotic often pluck their prey at perch sites near to the tree stands and vineyards. All known Black Spar- nest (Brown & Brown 1979). These remains were rowhawk nests have been systematically monitored identified to species level by comparing them with since 2000. At the time of this study (2015), the reference samples, by the shape and size of the nests of about 50 breeding pairs were known. During humerus, keel, coracoid and pelvic girdle, and from the breeding season (March–November), active feathers. Prey remains found at the nest-site may nests were located by surveying suitable stands of only represent a portion of what is being eaten by trees and known nesting sites and searching for Spar- adult Black Sparrowhawks, as other remains may rowhawks, prey remains, whitewash or nesting struc- be discarded elsewhere and some samples may be tures (see Martin et al. 2014a for details). When lost due to scavenging, decomposition, weather or chicks were between 3.5 and 4.5 weeks old, they cleaning (Rutz 2003, Drewitt & Dixon 2008). were individually colour-ringed, sexed, weighed and measured. Blood samples (maximum 1 mL) were Prey abundance: point counts. Bird counts were collected from the brachial vein, with either an insu- conducted at 116 sites to determine the abundance lin syringe or a needle (Gauge 29) and heparinized of prey species across a variety of habitat types capillary tubes. Blood smears were prepared and air- (Fig. 1). The sites were chosen such that each dried directly in the field. In this study we analysed habitat received similar sampling effort (Table S1). morphometric data from 343 nestlings. Blood sam- At each site, all birds seen and heard within a 150-m ples were taken from 250 nestlings from 66 nests. radius in a 15-min time period were counted. Two counts were conducted at each site, each count Estimation of health status about 3 months apart in either 2014 or 2015, giving All blood smears were fixed with methanol and a total of 232 individual counts (98 in May and stained with Giemsa’s stain following the standard August 2014 and 134 in September/October and protocol of Hemacolorâ Rapid staining of blood December 2015). As there was no significant smear kit (Merck, Darmstadt, Germany). The difference in abundance between the different survey slides were first scanned under a microscope at sessions within a year (GLM with negative binomial 409 magnification to determine the presence or errors: z = 1.64, df = 97, P = 0.1 and z = 0.51, absence of blood parasites, data that were later df = 131, P = 0.6 for 2014 and 2015, respectively), used to estimate the risk of infection in relation to the abundance of each species was calculated over all birds’ nest locations. For infected individuals, the months and years. Of the species recorded in the intensity of infection was then determined by scan- counts, only those which Black Sparrowhawks are ning each slide at 10009 magnification with an oil known to prey on (i.e. those observed in prey immersion lens and counting the number of para- remains in this study and documented in other sites seen within 10 000 erythrocytes. The infec- studies; Brown & Brown 1979, Malan & Robinson tion intensity can be seen as a measure of an 1999) were included in the analyses. individual’s susceptibility to the parasite. Simulta- neously, the proportion of each type of leucocyte Data analysis (heterophil, lymphocyte, basophil, eosinophil and monocyte) was determined to obtain the H/L ratio Defining the urban gradient (based on a minimum of 100 white blood cells). Land cover data were extracted from a 2013–14 To derive a body condition index we extracted South African National Land-Cover map obtained residuals from a second-order curve of tarsus through the South African National Biodiversity length on body mass and corrected for the Institute (http://bgis.sanbi.org/DEA_Landcover/

Figure 1. Google Earth image of point count sites (n = 116) covering a range of habitats throughout the Cape Peninsula study area. Each point was surveyed twice either in May and September 2014 or in October and December 2015. [Colour ﬁgure can be viewed at wileyonlinelibrary.com] project.asp). These data describe the cover of 72 habi- size (95% kernel density estimations) of Black Spar- tat categories at a 30-m resolution. Categories describ- rowhawks during the breeding season, using data from ing urban habitats (i.e. built-up, commercial, six GPS-tagged males (Sumasgutner et al. 2016c). industrial, residential) were grouped together to obtain the total percentage of urban cover within a 2-km buf- Statistical analyses fer around each nest, and thus were used to quantify the urbanization gradient. A buffer scale of 2 km was Effect of urbanization on health. Each health selected on the basis of estimates of the home-range parameter considered in this study (infection risk

and intensity for Haemoproteus and Leucocytozoon, analyses were conducted in R (R Core Team, H/L ratio, body condition index) was analysed as a 2015), using the MASS (Venables & Ripley 2002), response variable in a generalized linear mixed lme4 (Bates et al. 2015), effects (Fox 2003) and model (GLMM) using the urban gradient (% car (Fox & Weisberg 2011) packages. urban cover at each nest) as the main explanatory variable. For all GLMMs, the year, nest-site and Effect of urbanization on diet composition. Data from brood that each nestling was sampled from were prey remains collected over multiple years at the included as random terms to account for same territory were pooled to produce an pseudoreplication arising from several individuals aggregate description of diet for each nest-site and coming from the same nest between years or 10 prey categories were created based on the most multiple broods within the year, and multiple common prey items (Table 2). The diet breadth individuals from the same brood. All models were was calculated for each nest-site using the corrected for the age of the nestlings to account standardized Levins’ index (BA; Levins 1968, for differences in exposure time to parasites and Krebs 2004): other stressors. To do so, we used the residuals of a regression of sex on tarsus length because tarsus P1 1 length can be used as a proxy of age after pi2 BA ¼ accounting for sexual differences in tarsus length if N 1 the leg is not yet fully grown (Kostrzewa & Kostrzewa 1987, Hardey et al. 2006). A GLM where pi represents the proportion of the diet rep- comparing tarsus length and wing length, a more resented by each prey type and N is the number commonly accepted proxy for age in nestlings, of different prey categories. Since the standardized revealed that the two measurements were highly Levins’ index was normally distributed, we used a correlated (F = 14.19, P < 0.001) in chicks with a linear model with a Gaussian error structure to wing length of < 270 mm (88% of the 67 chicks analyse variation in diet breadth along the urban for which both measurements were available), gradient. For major prey items, pi was modelled as suggesting that tarsus length can be used as a a function of urban gradient using a binomial error substitute for wing length in correcting for age. structure. Tarsus length is therefore an imperfect proxy for To test for an effect of urbanization on the age in larger nestlings, but could not be replaced diet composition, we only considered the 26 by wing length, as wing measurements were only nest-sites for which we had seven or more prey available for 59 of the 247 nestlings used in the remain samples, as a rarefaction curve indicated study. For parasite infection risk and intensity, the this was sufficient for explaining 90% of the diet sex of the nestling was also included as a separate composition (Fig. S1). This yielded a sample size fixed effect to account for the known effect of sex of 795 prey samples and thus we lost very little on parasite susceptibility in this species (Lei et al. information from the full sample of remains 2013). A GLMM modelling nestling body (Table S7). condition as a function of brood size showed that brood size (i.e. possible intra-brood competition; Prey abundance between habitat types. Point count Gyllenberg et al. 2011, Sumasgutner et al. 2016a, data were used to calculate the average total 2016b) did not affect the body condition of abundance of all major prey species in each v2 = = nestlings ( 1; 114 0.77, P 0.4). This factor was habitat, as well as the average abundance of each therefore not included in further models involving prey species in each habitat type. For each prey body condition. The quantitative variables were species, we used (1) a Kruskal–Wallis test to assess standardized to set the variables in comparable whether the prey abundance differed between dimensions. Infection risk by each parasite was habitat types and (2) post-hoc Dunn tests (Dunn estimated using a binomial error structure 1964) to identify the habitat(s) in which the (presence–absence data), while infection intensity abundance was (were) significantly different. In was analysed with a negative binomial error step (2), the P-values were corrected using the structure, as these were over-dispersed count data. Bonferroni correction to account for the increased The mixed models for H/L ratio and body Type-I error due to multiple testing. Non- condition followed a Gaussian error structure. All parametric tests were used because data were non-

fi v2 = normal and because we could not nd any nest on either H. nisi infection risk ( 1; 112 transformations that enabled us to respect the 0.25, P = 0.62; Table 1, Fig. 3a) or infection inten- v2 = = assumptions of linear models used in the other sity ( 1; 20 2.33, P 0.13; Table 1, Fig. 3b). components of this study. For Leucocytozoon toddi, 52 of the 250 sampled nestlings were infected (prevalence of 21%), with an infection intensity ranging from 1 to RESULTS 254 parasites per 10 000 erythrocytes. There was no significant effect of urbanization Health and blood parasite infection on L. toddi infection intensity (v2 = 3.27, along the urban gradient 1; 42 P = 0.07; Table 1, Fig. 3d); however, infection risk Within the 82 nests used in this study, the urban declined significantly with increasing urban cover v2 = = gradient (% of urban cover within a 2-km radius ( 1; 112 4.43, P 0.04; Table 1; Fig. 3c). The of the nest) varied from 2 to 81% (Fig. 2). Among H/L ratio varied considerably among the individu- 250 nestlings, 25 were infected by Haemoproteus als, ranging between 0.08 and 3.65 (average nisi (i.e. a prevalence of 10%), with an infection 0.83 0.45 se), but it was not significantly influ- v2 = intensity ranging from 1 to 26 parasites per enced by the urban gradient ( 1; 113 0.26, 10 000 erythrocytes. We found no significant rela- P = 0.61; Table 1, Fig. 3e). Finally, the body con- tionship between the urban gradient around the dition index of 339 nestlings was not significantly

10 Number of nests

0 0-10 11-20 21-30 31-40 41-50 51-60 61-70 71-80 81-90 91-100 % Urban cover

Figure 2. Percentage of urban cover within a 2-km radius buffer around Black Sparrowhawk nests used in this study (n = 82).

Table 1. GLMMs exploring nestling health parameters (heterophil/lymphocyte ratio, body condition index and blood parasite infections) in relation to urban cover within 2 km around nest-sites, after correcting for the age and sex of the nestlings.

Variable Error structure n df Estimate se v2 P-value

Haemoproteus risk Binomial 250 112 0.20 0.41 0.25 0.62 Haemoproteus intensity Negative binomial 25 20 0.27 0.20 2.33 0.13 Leucocytozoon risk Binomial 250 112 0.56 0.27 4.43 0.04 Leucocytozoon intensity Negative binomial 52 42 0.43 0.25 3.27 0.07 Heterophil/lymphocyte ratio Gaussian 250 113 0.02 0.03 0.26 0.61 Body condition Gaussian 339 158 1.37 3.58 0.15 0.70

(a) P = 0.62 (b) P = 0.13 2.0 –3

1.5

–4 1.0 infection Risk infection intensity

–5 0.5

Haemoproteus –6 0.0 Haemoproteus

–0.5 –2 –1 0 1 2 –2 –1 0 1 2 % Urban cover % Urban cover (c) (d) P = 0.04 P = 0.07 4.0 0 3.5

–1 3.0

2.5 Infection intensity infection risk –2 2.0

1.5 –3 Leucocytozoon

Leucocytozoon 1.0

–4 0.5

–2 –1 0 1 2 –2 –1 0 1 2 % Urban cover % Urban cover (e) (f) 1.00 P = 0.61 P = 0.70 15 0.95 10

0.90 5

0.85 0

0.80 –5 Body condition

Heterophil/Lymphocyte ratio 0.75 –10

–15 0.70

–2 –1 0 1 2 –2 –1 0 1 2 % Urban cover % Urban cover

Figure 3. Health parameters of Black Sparrowhawk nestlings in relation to the percentage of urban cover within 2 km around the nest-site after correction for age and sex of the nestlings: (a) Haemoproteus infection risk, (b) Haemoproteus infection intensity, (c) Leucocytozoon infection risk, (d) Leucocytozoon infection intensity, (e) heterophil/lymphocyte ratio and (f) body condition index.

influenced by the urban gradient (P = 0.70, Prey abundance across habitats v2 = 0.15; Table 1, Fig. 3f). 1; 158 The Kruskal–Wallis tests indicated that the abun- Some of the health parameters were also age- dance of each of the main prey species, except and/or sex-dependent. Haemoproteus infection risk Speckled Pigeon, was significantly different across increased with age (estimated by the nestlings’ tar- habitat types (Fig. 4). After correction for multiple sus length corrected for sex; v2 = 12.29, 1; 112 testing, the Red-eyed Dove Streptopelia semitor- P < 0.001), and was higher in male than in female quata, the most important prey species, showed no nestlings (v2 = 40.69, P < 0.001). Conversely, 1; 112 significant differences. For some species, abundance females had significantly higher Haemoproteus was clearly higher in more transformed habitats. intensities (v2 = 4.39, P = 0.04) and a higher risk 1 Post-hoc Dunn tests showed for example that the of infection by Leucocytozoon (v2 = 6.89, 1; 112 abundance of all nine species combined and of P = 0.009). In addition, Leucocytozoon intensity Rock Doves alone was significantly higher in open and the H/L ratio decreased with nestlings’ age intensive and urban habitats than the other habitat (i.e. tarsus length). Detailed results for each model types (Table 4, Tables S8–S14). Some species were are shown in Tables S2–S6. abundant in both urban and non-urban landscapes, such as Laughing Dove Streptopelia senegalensis and Diet composition along the urban Cape Turtle Dove Streptopelia capicola. The habitat gradient types containing the fewest prey items (in terms of total numbers counted) were forests and gardens. Five species of doves and pigeons made up 87.2% (n = 729) of the 836 prey remains collected from 45 nest-sites between 2012 and 2015 (Table 2). DISCUSSION Other prey included Helmeted Guineafowl Numida Our results show that the health of Black Spar- meleagris (5.6%), Spotted Thick-knee Burhinus rowhawk nestlings does not appear to be nega- capensis (1.9%) and various other species (5.3%). tively impacted by urbanization in terms of Diet breadth ranged between 0.03 and 0.61 physiological and body condition or blood parasite (average 0.26 0.15 se) and was not significantly infection. There were also no obvious trends in influenced by the urban gradient (F = 1.09, diet composition along the urban gradient, suggest- P = 0.31; Table 3). When considering the propor- ing that Black Sparrowhawks benefit from food tion in the diet of the six main prey species (which resources of ample quantity and quality across dif- made up 92.8% of the diet), we found no signifi- ferent urban habitat types. This, together with the cant relationships between the proportion of any presence of prime nesting sites, may in part of the prey items and the urban gradient except explain why the species thrives in the urban envi- for Speckled Pigeons Columba guinea, which were ronment of Cape Town (Malan & Robinson 2001, less frequently preyed upon in more urban areas Rullman & Marzluff 2014). (v2 = 41.32, P = 0.01; Table 3).

Table 2. Species composition of all prey remains collected from nest-sites: number of collected items (n) and their proportion in the prey remains (%).

Species Latin name n % Cumulative %

Red-eyed Dove Streptopelia semitorquata 354 42.3 42.3 Rock Dove Columba livia 238 28.5 70.8 Speckled Pigeon Columba guinea 66 7.9 78.7 Helmeted Guineafowl Numida meleagris 47 5.6 84.3 Laughing Dove Streptopelia senegalensis 45 5.4 89.7 Cape Turtle Dove Streptopelia capicola 26 3.1 92.8 Spotted Thick-knee Burhinus capensis 16 1.9 94.7 Raptors Accipiter tachiro, Accipiter ruﬁventris 11 1.3 96.0 Starlings Sturnus vulgaris, Onychognathus morio 9 1.1 97.1 Other: Domestic chicken, Cape Spurfowl, Blacksmith Lapwing, Olive 24 2.9 100 Thrush, Hadeda Ibis, African Sacred Ibis, Grey Squirrel, Mole Rat spp.

Table 3. GLMs assessing whether diet breadth (measured by the Levins index) and the frequency of the six most common prey species within the diet varies with increasing urban cover surrounding the nest-site (F-tests for models with Gaussian error structure and chi-square tests for models with binomial error structures).

Error structure df Estimate se F/v2 P

Levins index Gaussian 24 0.002 0.002 1.09 0.31 Red-eyed Dove Quasibinomial 24 0.004 0.004 32.71 0.35 Rock Dove Quasibinomial 24 0.004 0.005 46.84 0.45 Speckled Pigeon Binomial 24 0.019 0.008 41.32 0.01 Helmeted Guineafowl Binomial 24 0.003 0.009 40.61 0.71 Laughing Dove Binomial 24 0.009 0.009 47.94 0.33 Cape Turtle Dove Binomial 24 0.009 0.012 34.40 0.47

9 main prey species Red-Eyed Dove Rock Dove χ2 P (χ2 = 44.31, P < 0.001) (χ2 = 15.45, P = 0.02) ( = 63.14, < 0.001) 35 5 16 30 14 4 25 12 20 3 10 8 15 2 6 10 1 4

Abundance per count Abundance per 5 2 0 0 0 FOLWGFVOIU FOLWGFVOIU FOLWGFVOIU

Speckled Pigeon Helmeted Guineafowl Laughing Dove Cape Turtle Dove χ2 P 2 (χ2 = 30.21, P < 0.001) χ2 P ( = 8.47, = 0.21) (χ = 21.49, P = 0.001) 2.5 ( = 13.59, = 0.03) 2.5 2.5 2.5 2 2 2 2

1.5 1.5 1.5 1.5

1 1 1 1

0.5 0.5 0.5 0.5 Abundance per count Abundance per 0 0 0 0 FOLWGFVOIU FOLWGFVOIU FOLWGFVOIU FOLWGFVOIU

Figure 4. Habitat-speciﬁc abundance observed for the bird species most commonly preyed on: Red-eyed Dove Streptopelia semitorquata, Rock Dove Columba livia, Speckled Pigeon Columba guinea, Helmeted Guineafowl Numida meleagris, Laughing Dove Streptopelia senegalensis and Cape Turtle Dove Streptopelia capicola. The x-axis represents a gradient from the most natural (left) to the most transformed or man-made habitat types (right): F, forest; OL, open landscape; W, wetland; G, garden; FV, ﬁeld/vineyard; OI, open intensive landscape; U, urban. Results of Kruskal–Wallis chi-square tests comparing prey abundance across all habitats are also shown (6 df).

Considering that early life experiences (i.e. con- completely dependent on their parents to provide ditions experienced during nestling stage) can be them with food. In certain circumstances, urban crucial for individual fitness (Lindstrom€ 1999), we prey might be of lower quality, for example due predicted negative health consequences for Black to insufficient dietary antioxidants or an imbalance Sparrowhawk nestlings being reared in heavily in fatty acid composition (Isaksson 2015, Toledo urbanized areas. Nestlings are expected to be par- et al. 2016), poor body condition (as a result of ticularly vulnerable to stressors in urban environ- feeding on urban ‘junk food’; Shochat 2004) or ments because they are confined to their nests and due to infection with diseases or parasites that do not have the option to avoid any adverse condi- might be transmitted to the predator (Estes & tions they are exposed to. Thus they might exhibit Mannan 2003). Our results do not support these symptoms of physiological stress. Nestlings are also predictions.

Infection risk and intensity for Haemoproteus and infection intensity by Leucocytozoon were not signiﬁcantly affected by the amount of urban cover s in abun- surrounding nest-sites. In fact, the risk of Leucocy- tozoon infection was lower in more urbanized nests. We can therefore add to a number of studies (e.g. Delgado & French 2012) that have found 3.78)** 3.19)*

mixed effects of urbanization on parasite infection, ( supporting the observation that the pattern may vary depending on the host–parasite system under 4.99)*** ( consideration and on the transmission mode of the parasite (Brearley et al. 2012, Giraudeau et al. 2014). When the parasite is transmitted trophi- 9 main species ( C. livia S. senegalensis cally (i.e. by consumption of an infected individual), urban raptors feeding on hyper-abundant urban species like pigeons may be more prone to 4.02)*** 4.52)*** 3.44)**

’

( infection than rural ones, as seen in Cooper s Hawks Accipiter cooperii infected with Trichomonas 4.20)*** 5.06)*** (Estes & Mannan 2003). However, in the case of ( ( vector-borne parasites, such as the haemosporidian 0.001).

< parasites studied here, the effect of urbanization P 9 main species ( C. livia 9 main species ( C. livia S. senegalensis on their prevalence is likely to depend on the *** effect of urbanization on their vectors. Biting midges can breed in a wide range of habitats (e.g. 0.01,

< pools, streams, swamps, tree holes, irrigation 4.22)*** 5.26)*** 4.22)*** P ( pipes) as long as there is enough water/moisture ** (Mellor et al. 2000), but blackflies require running 0.05, 4.48)*** 5.33)*** water and high-velocity streams (Rivers-Moore < ( ( et al. 2007). We therefore suggest that blackflies P * may be less abundant in highly urbanized areas, 9 main species ( C. livia C. livia S. senegalensis perhaps explaining why birds are less at risk of infection by Leucocytozoon in these areas. Similarly, there were no significant relationships between urbanization and body condition or the (4.02)*** 2.89)* H/L ratio in Black Sparrowhawk nestlings. The ( absence of any negative impacts of urbanization on cant results are shown (

fi the condition and H/L ratio of nestlings may fur- (5.46)*** (3.21)* ther explain why urbanization does not affect the birds’ susceptibility to haemosporidian parasites C. livia S. senegalensis C. livia N. meleagris (Heath & Dufty 1998). Together, these results suggest that the health of Black Sparrowhawk nestlings is not affected by urban stressors connected to the high density of buildings and traffic structures. (4.30)***Using a rural 9 main species ( –urban gradient approach may therefore be insufficient in explaining the mechanisms (4.59)*** (4.16)***

statistic is given and only signi behind the health of city-dwelling species. The fac- Open intensive Urban Forest Garden Open landscape Field/vineyard z tors that contribute towards the health of an indi- 9 main species (3.69)** 9 main species (4.27)*** N. meleagris C. livia C. livia vidual may go beyond the degree of urban cover, ﬂ

Results of Dunn tests run for each of the main prey species and for the cumulative abundance of the nine main prey species to test for pairwise difference and instead consist of a multitude of in uences and environmental features (Hahs & Evans 2015).

x A mechanism by which urbanization could ~ intensive vineyard landscape The value of the Open Wetland Garden Field/ Open Urban Table 4. dance between habitats. y affect the health and condition of predatory birds

is through their diet if urbanization prevents them stability and reliability of prey across different from accessing prey in high enough quantities or habitat types (Mannan & Boal 2004) and times of of good nutritional quality (e.g. Sternalski et al. year (this study). This can be a major contributing 2010, Terraube et al. 2011 for natural systems and factor to the persistence of raptors in altered land- Sumasgutner et al. 2014 for an urban setting). scapes. Reliable availability of a variety of prey Insufficient prey or prey of insufficient quality species allows Crowned Eagles in Durban, South might decrease the condition of the nestlings or Africa (Reeves & Boshoff 2015), and Verreaux’s increase physiological stress (Andersson et al. Eagles Aquila verrauxii in transformed agricultural 2015). In addition, bioaccumulation of contami- habitat in the Western Cape (Murgatroyd et al. nants acquired from prey species can be detrimen- 2016) to withstand the impacts of landscape tal to raptors, as seen in Cooper’s Hawk, Sharp- change. shinned Hawk Accipiter striatus (Elliot & Martin In the case of the Black Sparrowhawk and other 1994), Barn Owl Tyto alba, Common Buzzard congeners with similar foraging strategies, urban Buteo buteo and Tawny Owl Strix aluco (Lopez- habitats may also provide ideal foraging land- Lopez et al. 2001). Conversely, the lack of an scapes, providing features such as edges, fence effect of urbanization on raptors’ health status as lines, perches and tree cover from which to hunt observed here may result from birds being able to (Bolger 2001, Rutz 2006, Rullman & Marzluff maintain a diet of similar quality along the urban 2014). This may also explain the lack of trend in gradient. To answer this question, we attempted diet and prey abundance with urbanization. This to determine whether urban Black Sparrowhawks has been found in Peregrine Falcons Falco peregri- had a distinct ‘urban diet’, dominated for instance nus in Cape Town (Jenkins & Benn 1998). by feral pigeons and other doves, and, as a result, Although Peregrines clearly benefit from the abun- a decreased diet breadth. This was based on forag- dance of prey within urban Cape Town, their ing theories that predict that diet diversity capacity to access this rich resource is dependent decreases as the abundance of the most favoured on the structure of the urban habitat and presence prey items increases (Stephens & Krebs 1986, of appropriate structures for hunting successfully Sodhi & Oliphant 1993). Conversely, we expected (Jenkins & Benn 1998). Thus, the diverse urban other prey species that might be less tolerant of and suburban habitats may provide ideal hunting urbanization to feature more in the diet of birds in grounds for Black Sparrowhawks, which tend to less urban habitats, resulting in an increase in diet ambush prey from a hidden perch (Brown & breadth. This has been witnessed in congeners of Brown 1979), so habitat edges might be more the Black Sparrowhawk, such as Cooper’s Hawk, important than habitat type. In addition, minor where the diet of urban birds was composed pri- changes in urban cover may mean little to a highly marily of doves, whereas rural birds caught a mobile species such as Black Sparrowhawk when greater variety of prey (Estes & Mannan 2003). the city is scattered with patches of suitable habi- However, our results show that the diet of Black tat and contains an abundant supply of prey. Thus, Sparrowhawks differs little along the urbanization the heterogeneous environment of Cape Town gradient, in terms of both diet breadth and the may mask the effect of an urban gradient. quantity of preferred prey consumed by the birds. Our study supports the ‘predation paradox’ All major prey species together and some spe- observed in urban areas (Shochat 2004), whereby cies in particular (e.g. Rock Dove, Helmeted Gui- predator populations increase in urban areas while neafowl) were more abundant in urban habitats, overall predation pressure remains lower than in whereas other prey (e.g. Red-eyed Dove and Cape non-urban areas, due to the hyper-abundance of Turtle Dove) were also abundant in less urban (avian) prey species in cities (McKinney 2006, habitat types. Therefore, overall, prey abundance Fischer et al. 2012). Bird-eating raptors usually was well spread across all habitat types considered, experience decreased hunting success and energy particularly that of Red-eyed Doves, the most returns for the time they spend foraging (Temeles important prey species of Black Sparrowhawks. 1985, Jenkins & Hockey 2001) but in urban areas This may explain the lack of any trends in diet there is no shortage of hunting opportunities and a composition. These findings suggest that Black potentially higher likelihood of success. This may Sparrowhawks are under little nutritional stress, in turn have repercussions for the individual health due both to the abundance of prey and to the of these predators. Body condition is often used as

an indicator of energy reserves accumulated in the Faculty Animal Ethics Committee (permit number: nestling stage (Constantini et al. 2009). Birds with 2012/V37/AA). All procedures were in line with South a higher body condition have in turn been shown African legal requirements, and the necessary permits to respond and adapt more rapidly to causes of for monitoring, capturing and ringing birds were acquired from Cape Nature and South African National physiological stress compared with individuals in Parks. We are grateful to the Black Sparrowhawk team – poorer condition, minimizing the physiological Johan Koeslag, Mark Cowen, Gareth Tate, Margaret impacts of disturbance, pollutants, disease and Maciver and Sharon Pryce – for the long-term popula- nutritional stress (Heath & Dufty 1998). tion monitoring and data collection. Denise Hamerton These feedbacks between urban habitat charac- and Jofred Opperman from the Iziko National Museum teristics, prey abundance and individual health of Natural History provided comparative material for fi allow us to hypothesize a potentially positive the identi cation of prey remains. Bruce Baigrie analysed prey remains samples from 2012 and 2013 and Graham effect of cities on bird-eating raptors such as Black Avery assisted with identification of prey remains. Gab- Sparrowhawks, suggesting that the abundance of riella Leighton, Michelle Maritz and Elelwani Musekwa prey in cities may override potential negative helped with analysing blood slides and compiling the impacts of urbanization on health due to distur- parasite and leucocyte database. Caroline Isaksson pro- bance or other sources of stress. This is not surpris- vided valuable input on the project. 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Sodhi, N.S. & Oliphant, L.W. 1993. Prey selection by urban- SUPPORTING INFORMATION breeding merlins. Auk 110: 727–735. Solonen, T. & Ursin, K.A. 2008. Breeding of Tawny Owls Additional Supporting Information may be found Strix aluco in rural and urban habitats in southern Finland. in the online version of this article: Bird Study 55: 216–221. Table S1. Descriptions of habitat types and the Stephens, D.W. & Krebs, J.R. 1986. Foraging Theory. number of sites within each of them at which Princeton, NJ: Princeton University Press. Sternalski, A., Mougeot, F., Eraud, C., Gangloff, B., Villers, point counts were conducted (N). A. & Bretagnolle, V. 2010. Carotenoids in nestling Table S2. GLMM modelling the effects of sex, Montagu’s Harriers: variations according to age, sex, body age (quantified using the residuals of a regression condition and evidence for diet-related limitations. J. Comp. between tarsus length and sex) and urban cover on – Physiol. B. 180:33 43. the risk of infection by Haemoproteus nisi in Black Sternalski, A., Mougeot, F. & Bretagnolle, V. 2012a. Carotenoid limitation and allocation priorities in asynchronous Sparrowhawk nestlings. raptor nestlings. Biol. J. Linn. Soc. 105:13–24. Table S3. GLMM modelling the effects of Sternalski, A., Mougeot, F., Perez-Rodr ıguez, L. & sex, age (quantified using the residuals of a Bretagnolle, V. 2012b. Carotenoid-based coloration, regression between tarsus length and sex) and condition, and immune responsiveness in the nestlings of a urban cover on the intensity of infection by sexually dimorphic bird of prey. Physiol. Biochem. Zool. 85: 364–375. Haemoproteus nisi in Black Sparrowhawk Stout, W.E., Temple, S.A. & Cary, J.R. 2006. Landscape nestlings. features of Red-tailed Hawk nesting habitat in an urban/ Table S4. GLMM modelling the effects of suburban environment. J. Raptor Res. 40: 181–192. sex, age (quantified using the residuals of a Sumasgutner, P., Nemeth, E., Tebb, G., Krenn, H.W. & regression between tarsus length and sex) and Gamauf, A. 2014. Hard times in the city – attractive nest sites but insufficient food supply lead to low reproduction urban cover on the risk of infection by Leucocy- rates in a bird of prey. Front. Zool. 11: 48. tozoon toddi in Black Sparrowhawk nestlings. Sumasgutner, P., Millan, J., Curtis, O., Koeslag, A. & Amar, Table S5. GLMM modelling the effects of A. 2016a. Is multiple nest building an adequate strategy to sex, age (quantified using the residuals of a cope with inter-species nest usurpation? The case of Black regression between tarsus length and sex) and Sparrowhawks (Accipiter melanoleucus) and Egyptian Geese (Alopochen aegyptiaca). BMC Evol. Biol. 16:1–11. urban cover on the intensity of infection by Sumasgutner, P., Tate, G.J., Koeslag, A. & Amar, A. 2016b. Leucocytozoon toddi in Black Sparrowhawk Family morph matters: factors determining survival and nestlings. recruitment in a long-lived polymorphic raptor. J. Anim. Ecol. Table S6. GLMM modelling the effects of age – 85: 1043 1055. (quantified using the residuals of a regression Sumasgutner, P., Tate, G., Koeslag, A. & Amar, A. 2016c. Seasonal patterns in space use of Black Sparrowhawks between tarsus length and sex) and urban cover Accipiter melanoleucus breeding in an urban environment. on the heterophil/lymphocyte ratio in Black Bird Study 63: 430–435. Sparrowhawk nestlings. Temeles, E.J. 1985. Sexual size dimorphism of bird-eating Table S7. Diet composition (number of items – hawks: the effect of prey vulnerability. Am. Natur. 125: 485 from different prey species out of the total prey 499. Terraube, J., Arroyo, B., Madders, M. & Mougeot, F. 2011. number of prey remains from each nest-site Diet specialisation and foraging efficiency under fluctuating (N)), diet breadth and percentage of urban cover vole abundance: a comparison between generalist and at 26 Black Sparrowhawk nest-sites. specialist avian predators. Oikos 120: 234–244. Table S8. Results of the Dunn test comparing Toledo, A., Andersson, M.N., Wang, H.-L., Salmon, P., the total abundance of the nine main prey Watson, H., Burdge, G.C. & Isaksson, C. 2016. Fatty acid profiles of Great Tit (Parus major) eggs differ species of Black Sparrowhawks in each pair of between urban and rural habitats, but not between habitat types (*P < 0.05, **P < 0.01, coniferous and deciduous forests. Sci. Nat. 103: 55. ***P < 0.001). Valkiunas, G. 2005. Life cycle and morphology. In Avian Table S9. Results of the Dunn test comparing Malaria Parasites and Other Haemosporidia. Boca Raton, the abundance of Red-eyed Doves Streptopelia FL: CRC Press. Venables, W.N. & Ripley, B.D. 2002. Modern Applied semitorquata in each pair of habitat types Statistics with S, 4th edn. New York: Springer. (*P < 0.05, **P < 0.01, ***P < 0.001). Table S10. Results of the Dunn test compar- Received 13 June 2016; ing the abundance of Rock Doves Columbia livia revision accepted 10 October 2016. in each pair of habitat types (*P < 0.05, Associate Editor: Jose Antonio Sanchez-Zapata. **P < 0.01, ***P < 0.001).

Table S11. Results of the Dunn test senegalensis in each pair of habitat types comparing the abundance of Speckled Pigeons (*P < 0.05, **P < 0.01, ***P < 0.001). Columba guinea in each pair of habitat types Table S14. Results of the Dunn test compar- (*P < 0.05, **P < 0.01, ***P < 0.001). ing the abundance of Cape Turtle Doves Strep- Table S12. Results of the Dunn test compar- topelia capicola in each pair of habitat types ing the abundance of Helmeted Guineafowl (*P < 0.05, **P < 0.01, ***P < 0.001). Numida meleagris in each pair of habitat types Figure S1. Rarefaction curve to determine the (*P < 0.05, **P < 0.01, ***P < 0.001). minimum number of samples required to explain Table S13. Results of the Dunn test compar- 90% of diet composition at a given nest-site. ing the abundance of Laughing Doves Streptopelia