Behavioral Evidence of Hunting and Foraging Techniques by a Top Predator Suggests the Importance of Scavenging for Preadults

Received: 16 December 2016 | Revised: 1 March 2017 | Accepted: 5 March 2017 DOI: 10.1002/ece3.2944

ORIGINAL RESEARCH

Behavioral evidence of hunting and foraging techniques by a top predator suggests the importance of scavenging for preadults

1Department of Animal Science, Faculty of Life Sciences and Engineering, University of Lleida, Abstract Lleida, Spain Scavenging may be a regular feeding behavior for some facultative raptor species oc- 2 Division of Conservation Biology, Institute cupying low quality habitats and/or with little experience in hunting techniques. of Ecology and Evolution, University of Bern, Bern, Switzerland However, its importance has been largely underestimated due to methodological limi- 3Department of Mathematics, Faculty of Life tations in identifying the real proportion in the diet. Here, through direct observations, Sciences and Engineering, University of Lleida, we assessed the hunting and foraging success of the threatened Spanish imperial Lleida, Spain 4Fundación CDB-Habitat, Madrid, Spain eagle Aquila adalberti determining the influence of age, sex, breeding status, habitat 5Boscaje S.L., Segovia, Spain quality, prey type, and landscape characteristics. From 465 observations, Spanish im- 6Deputy General Directorate on perial eagles used hunting in flight (42%), scavenging (30%), hunting from a perch (16%) Nature, Spanish Ministry of Agriculture, Food and kleptoparasitism (12%). Our model suggests that Prey size and Prey type best ex- and Environment, Madrid, Spain plain hunting success, followed by Landscape and Sex. Our findings suggest that Correspondence Spanish imperial eagles increase hunting success with age, with scavenging and klep- Antoni Margalida, Department of Animal Science, Faculty of Life Sciences and toparasitism regularly used as juveniles. The absence of relationships with any of the Engineering, University of Lleida, Lleida, Spain. variables considered suggests that kleptoparasitism is an opportunistic behavior used Email: [email protected] sporadically. Scavenging is also independent of habitat quality and landscape characteristics. Accordingly, low prey density is not a driver of carrion use for preadult individuals, suggesting that a lack of hunting ability obliges this age-class to use this alternative feeding technique regularly. As a result, the threatened Spanish imperial eagle population is also prone to mortality related to the illegal use of poison baits and, potentially, veterinary drugs (i.e., diclofenac).

KEYWORDS attack techniques, carrion consumption, facultative raptors, habitat quality, kleptoparasitism, Spanish imperial eagle

1 | INTRODUCTION scavengers (see a review in DeVault et al., 2003, 2016). In terrestrial ecosystems, although obligate scavengers are the main consumers Carrion consumption is a key ecological process influencing population of carrion remains, in the absence of some obligate scavengers such dynamics, community structure, and ecosystem functioning (DeVault, as vultures, a higher use of carrion by facultative scavengers occurs Rhodes, & Shivik, 2003; Selva & Fortuna, 2007). Carrion resources (DeVault et al., 2003; Moreno-Opo, Trujillano, & Margalida, 2016; are ephemeral and extensively used by vertebrates, mainly obligate Ogada, Torchin, Kinnaird, & Ezenwa, 2012).

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www.ecolevol.org | 1 Ecology and Evolution. 2017;1–8. 2 | MARGALIDA et al.

For some vertebrate facultative predators, such as raptors, the 1991; Sánchez, Margalida, González, & Oria, 2009; Sánchez et al., importance and ecological influence of scavenging has largely been 2008). The abundant literature is in contrast with the scarce informa- underestimated (DeVault & Rhodes, 2002; DeVault et al., 2003; tion available about hunting techniques and feeding behavior (see re- Sánchez-Zapata et al., 2010). This is due to the inherent biases of views in Ferrer, 1993; González, 1991; González & Margalida, 2008). methods used to assess the diet of raptor species, which generally In a recent study, which analyzed the size and selection of hunting underestimate the presence of carrion and other less conspicuous zones exploited by the species to obtain feeding resources (Fernández, remains that are difficult to identify (Redpath, Clarke, Madders, & Oria, Sánchez, González, & Margalida, 2009), no additional informa- Thirgood, 2001; Margalida, González, et al., 2007; Margalida, Sánchez, tion was obtained about differences in age classes in hunting tech- González, Oria, & Prada, 2007; Sánchez, Margalida, González, & Oria, niques or prey selection. Indirectly, it has been documented that the 2008). However, several studies have revealed that scavenging is more presence of nonadult individuals in breeding pairs implies a lower prevalent than traditional theory implies (Beasley, Olson, & DeVault, breeding output (Margalida et al., 2008) and that habitat quality influ- 2012; DeVault et al., 2003; Hammerschlag et al., 2016; Wilson & ences breeding success (Margalida, González, et al., 2007; Margalida, Wolkovich, 2011). The use of camera traps and video-cameras has Sánchez, et al., 2007; Margalida et al., 2008). Males assume hunting provided new and more objective tools to assess the diet of some fac- responsibilities and are the main providers of food to the nest, as ultative avian scavengers, demonstrating the importance of carrion in their smaller body size and other adaptations give them greater agility their diet (Moreno-Opo, Trujillano, Arredondo, González, & Margalida, and maneuverability to improve hunting success (Margalida, Sánchez, 2015; Moreno-Opo et al., 2016; Sánchez-Zapata et al., 2010) and et al., 2007). In addition, supplementary feeding for the species (i.e., the important role of facultative scavengers as facilitators of social dead rabbits provided near nesting sites) is a management tool that information transfer leading to nontrophic interactions among spe- demonstrates that the species can consume carrion regularly, increas- cies (Kane, Jackson, Ogada, Monadjem, & McNally, 2014; Moleón, ing through this technique breeding success, mainly in low quality Sánchez-Zapata, Selva, Donázar, & Owen-Smith, 2014). territories and pairs including inexperienced (i.e., subadult) individuals According to the Optimal Foraging Theory (MacArthur & Pianka, (González, Margalida, Oria, & Sánchez, 2006; González, Oria, et al., 1966; Schoener, 1971), predators prefer profitable prey in terms of 2006). Accordingly, scavenging could be a regular feeding behavior for energy efficiency to maximize fitness, usually net energy intake (Pyke, some facultative raptor species occupying low quality habitats and/or Pulliam, & Charnov, 1977). However, when the abundance of pre- when the individuals are inexperienced. Thus, it is necessary to assess ferred prey (due to its high profitability) diminishes, the predator can the influence of age, habitat quality, and landscape characteristics on use alternative preys (Steenhof & Kochert, 1988). Under these cir- the frequency of scavenging in the diet of this species to know their cumstances, the use of alternative techniques, such as scavenging or relevance in their trophic ecology. kleptoparasitism, can be beneficial to mitigate the absence of prey or Given this background, we hypothesized that immature and less low hunting success as a consequence of inexperience (Brockmanhn experienced individuals (mainly males) can have lower success on & Barnard, 1979; Halley & Gjershaug, 1996). Apart from indirect stud- hunting techniques and, as a result, use alternative techniques (i.e., ies on the diet determined through pellet analysis or remains found kleptoparasitism, scavenging) to optimize foraging success. Here, our at nesting sites (Real, 1996; Sánchez et al., 2008), information about goals are to assess the hunting success of Spanish imperial eagles scavenging behavior in raptor species other than vulture is scarce and and to determine whether different hunting techniques and foraging rarely quantified. For example, Sánchez et al. (2008) found that carrion success differs according to age, sex, breeding status, habitat quality, consumption ranged between 2% and 5% according to different diet prey type, and landscape characteristics. In addition, we estimate the assessment methods in breeding Spanish imperial eagles Aquila adal- importance of other feeding techniques (kleptoparasitism and scav- berti. On the other hand, Sánchez-Zapata et al. (2010), with the help enging) to obtain food resources, discussing the implications from a of automatic cameras, identified golden eagles Aquila chrysaetos on behavioral and conservation perspective. 24 (57%) of 42 monitored carcasses, with similar presence throughout the year. This suggests that the role of carrion in the feeding 2 | METHODS habits of facultative scavenger raptors may be more important than estimated. However, with respect the exposition to pathogens and 2.1 | Study area toxic by-products of microbial metabolism, obligate scavengers seem have more natural antibodies against botulinum toxin than do facul- The study was carried out within the framework of the Recovery tative scavengers (Blumstein, Rangchi, Briggs, Souza de Andrade, & Plans for this species in the Autonomous Communities of Castilla y Natterson-Horowtiz, 2017; Ohishi, Sakaguchi, Riemann, Behymer, & León, Castilla-La Mancha, Madrid and Extremadura. The majority of Hurvell, 1979). breeding birds inhabit plains and mountain ranges with patches of Spanish imperial eagles are distributed throughout the west- Mediterranean forest and “dehesa,” a kind of open forest of Quercus central quadrant of the Iberian Peninsula (González et al., 2008). They rotundifolia and Q. suber. Annually, the species’ breeding sites were are large, highly territorial raptors that feed upon medium-sized birds visited at least once a week between the months of January and and mammals. Most studies about their diet suggest that their main August (Margalida, González, et al., 2007; Margalida, Sánchez, et al., prey is the wild rabbit Oryctolagus cuniculus (Ferrer, 1993; González, 2007). Generally the visits started in January, coinciding with the time MARGALIDA et al. | 3 when the eagles were rebuilding their nests. The monitoring of the 2.3 | Attack success and foraging success territories ended in August, when the chicks left the nest. However, sporadic visits out the breeding period were also carried out coincid- We recorded behavior as a food-obtaining attempt (hunting in flight ing with the monitoring of marked individuals (González, Margalida, or from perching, kleptoparasitism, or scavenging) when an individual et al., 2006; González, Oria, et al., 2006). was observed prospecting the territory or perching and performing any of these actions (i.e., hunting techniques in flight or perched, kleptoparasitic interactions or carrion consumption). For each ob- 2.2 | General approach servation, we noted the following information: day, hour, individual, Between January 1990 and December 2013, 465 Spanish imperial sex, breeding status, habitat quality, habitat characteristics, hunting eagle hunting attacks (in flight or from a perch), kleptoparasitic ac- or feeding technique used, success of the feeding/hunting technique, tions, or scavenging (feeding behavior) were recorded by direct ob- and prey. We considered a successful attack or kleptoparasitic inter- servation. Observations were made within each area in conditions of action when the individual captured the prey as a result of the hunting good visibility from vantage points. Within study areas, observations technique used. were made throughout the entire year. All hunting attacks were re- A hunting attack was defined as direct rapid flight toward a clearly corded during monitoring of nesting territories (n = 86) and by ob- identifiable prey (Cresswell, 1994), and a capture was an attack that serving floater individuals (n = 199) in the study area (>2,000 h of resulted in the raptor catching hold of the prey (Cresswell & Quinn, fieldwork). All observations were made by the same observer (RS). 2004). Kleptoparasitic actions included interspecific kleptoparasitism Observations consisted of making scans noting the predator, the prey, (stealing food from other species) and intraspecific kleptoparasit- and/or the groups of prey within a radius of 400–500 m around the ism (stealing food from other Spanish imperial eagles). This feeding observer (Altmann, 1974; Kitowski, 2003). technique differs from scavenging because kleptoparasitism involves the opportunistic or habitual stealing of food items from other ani- TABLE 1 Definition of the variables used in models to analyze mals, generally interacting in flight or perching sites, whereas during attack success and feeding behavior for Spanish Imperial Eagles scavenging, the carrion consumption can be carried out by several

SEX: Sex of the individual. Male or female. Nondetermined individuals individuals that can consume carrion (always in the ground) without in- are not considered teracting among them. For analytical purposes, both were analyzed by AGE: Age of the individual. Categorical variable with three age- pooling as a consequence of limited data. In this way, every hunting at- classes: adults, subadults, and juveniles tack or kleptoparasitic action was classified as a success or failure. For ATTACK/FEEDING MODE: Categorical variable with two classes: (1) scavenging behavior, all the observations were considered successful prospecting flight and (2) from a perch. Kleptoparasitism and because in all cases the individual accessed the carrion source. All cap- scavenging behavior were analyzed separately ture attempts with undetermined outcomes were excluded from the PREY SIZE: Prey group size. Discrete quantitative variable analysis (Collopy, 1983). (range < 50 gr to >1 kg) Overall, 8 of 465 (1.7%) attempts by eagles were of unknown cap- PREY-TYPE: Corresponds to mammals, reptiles, birds, and other ture success due to distance from the observer and/or local topogra- (nonidentified) phy. Attacks by individuals whose sex could not be determined were BREEDING STATUS: Breeding status of the individual. Breeding vs. nonbreeding excluded from the analysis (Collopy, 1983). Eight variables were recorded for each attack (Table 1). The age of HABITAT QUALITY: Habitat type according to rabbit density. Categorical variable with two classes: high quality vs. low quality the individuals was classified into three categories in agreement with LANDSCAPE: Habitat characteristics according to vegetation plumages described by González et al. (2008): (1) juveniles from the structure and humanization. Categorical variable with four types: 1) first and second year, (2) immatures and subadults (“damero,” “dam- closed areas (forest formations and shrubland or Mediterranean ero avanzado,” and imperfect adult) and (3) adults (Table 2). To identify forest), open areas (without tree or shrub vegetation, and steppe individuals, we took into account the leg-rings, radio-tracked individ- areas, cereal crops, and grasslands), forest-open dehesas (forest areas and areas cleared of vegetation, pastures, and areas of scattered uals, or the characteristics of the plumage (see Bortolotti, González, bushes) and humanized areas Margalida, Sánchez, & Oria, 2008; González & Margalida, 2008). In the

TABLE 2 Sexual differences (M: male; F: female) in hunting/feeding techniques used by Spanish imperial eagles according to their age (A: adult; S: subadult; J: juvenile). Percentage appears in brackets

Flight Perch Kleptoparasitism Scavenging

A S J A S J A S J A S J Total

M 37 (52) 68 (61) 8 (16) 16 (22.5) 22 (20) 4 (8) 6 (8.5) 5 (4.5) 11 (22) 12 (17) 16 (14) 28 (55) 233 F 35 (53) 8 (32) 8 (19) 16 (24) 3 (12) 2 (5) 4 (6) 4 (16) 18 (43) 11 (17) 10 (40) 14 (33) 133 4 | MARGALIDA et al. case of adults, this allowed us to differentiate between breeding and TABLE 3 Summary of eight more simple models of success in nonbreeding individuals. hunting according to the studied variables. Models are shown, The type of attack was defined by the position of the eagle at the including the size sample (n), number of parameters (K), AIC correct values, Δi = AICc –AIC min values and Akaike weights (wi), based on beginning of the attack (from a perch or in flight). We categorized two c AICc. Models are ordered in terms of Δi for AICc different hunting techniques to obtain food: in flight and from perching. In addition, we separately analyzed the interactions with dead Model n K AICc Δi Wi prey. In this case, we analyzed the success of kleptoparasitic actions θSex 228 3 313.81 0.00 1.00 and the factors (i.e., landscape, habitat quality) affecting scavenging θPrey size 264 9 347.86 34.05 0.00 behavior (Table 1). θPrey type 268 4 352.61 38.80 0.00 With respect to the species hunted or fed upon (scavenging or θAge 268 4 365.73 51.92 0.00 kleptoparasitic actions), prey were grouped into three categories: θLandscape 268 7 369.27 55.46 0.00 mammals, birds, and reptiles. These categories were also subdivided θHabitat quality 267 3 371.46 57.65 0.00 according to prey size into six categories including prey of <50, 51– θBreeding status 267 4 372.13 58.33 0.00 100, 101–300, 301–600, 601–1,000, and >1,000 g. θ 268 3 373.42 59.61 0.00 To determine habitat quality, we used the same methodology as Technique González et al. (2008) considering high quality habitat when more than one rabbit/hectare was found and low quality when the density TABLE 4 Summary of eight more simple models of success in was below one rabbit/hectare. To categorize the different charac- hunting techniques according to the studied variables. Models are teristics of the habitats in which the hunting/feeding took place, we shown, degrees of freedom (df), Deviance and significance level considered the following habitats: closed areas (forest formations and model (p-value) shrubland or Mediterranean forest), open areas (without tree or shrub Model df Deviance p-value vegetation, and steppe areas, cereal crops and grasslands), the “dehesas” (forest areas cleared of vegetation, pastures and areas of scattered Sex 1 5.75 .017 bushes), and finally humanized areas. Prey size 7 30.67 <.0001 Prey type 2 15.36 <.0001 Age 2 3.40 .183 2.4 | Statistical analyses Landscape 2 9.80 .007 Following the methodological approach outlined by Burnham and Habitat quality 1 0.43 .512 Anderson (2002), we used the set of variables shown in Table 1 to de- Breeding status 1 0.04 .832 velop eight a priori hypothesized models to explain attack success. The Technique 5 12.54 .028 strategy of selecting a reduced set of candidate models guards against the risk of overfitting and finding spurious relationships (Johnson & Omland, 2004). We used generalized linear models (GLMs) to examine the effects of the selected variables on hunting success. With a GLM, 3 | RESULTS we studied 50 individual kleptoparasitic interactions assessing whether Sex, Age, Landscape, Habitat, or Breeding status affected the success Spanish imperial eagles obtained food through: hunting in flight of kleptoparasitism. Attack success was modeled as a binary variable in 194 (41.7%) of the cases, hunting from a perch in 73 (15.7%), (1 = success, 0 = failure). We used a logit link function (with binomial kleptoparasiting in 57 (12.3%), and scavenging in 141 occasions error distribution) for attack success models and to assess the effects of (30.3%). sex, age-class, prey characteristics, breeding status, and habitat features on the attack/feeding mode used as a response variable (see Table 1). 3.1 | Influence of age-class on feeding behavior and The significance of the parameters was studied with the Wald’s test. hunting techniques To determine the model that best explains hunting success, we analyzed the Akaike criteria and the deviance from the model. We fol- We found significant differences among age-classes on the feed- 2 lowed an information-theoretic approach in the analyses of our data ing techniques used (χ = 110.05, df = 6, p < .0001). Juveniles used (Burnham & Anderson, 2002). Model comparisons were based on the scavenging (61%) more frequently than adults (16.3%) and subadults bias-corrected version of Akaike’s information criterion (AICc) and (22.7%). In addition, juveniles used kleptoparasitism (61.4%) more than were ranked using AICc differences (∆i) and Akaike weights (wi). We adults (19.3%) and subadults (19.3%) (Table 2). On the contrary, the initially tested and compared the base models in Tables 3 and 4. Using technique more frequently used by adults was hunting in flight (52.6%) the obtained information, we then examined four models (Tables 5 followed by hunting from a perch (23.4%) and scavenging (16.8%). In and 6) that included the most important related variables. We did not the case of subadults, hunting in flight was also the most used tech- study quadratic models as we did not have available data. Analyses nique (56.7%) followed by scavenging (19.4%) and hunting from a were performed with the R program (16 R 2.10.1). perch (17.2%). MARGALIDA et al. | 5

TABLE 5 Summary of the four models Model n K AICc i W obtained by combining the most significant Δ i variables. Models are shown, including the θsex+Prey size+Prey type+Landscape 224 13 274.23 0.00 0.55 sample size (n), number of parameters (K), AIC θPrey size+Prey type+Landscape 224 12 274.74 0.51 0.42 correct values, Δi = AICc−AIC min, values, c θ 224 9 280.18 5.95 0.03 and Akaike weights (wi), based on AICc. Prey type+Prey size θ Models are ordered in terms of Δi for AICc Prey size+Landscape 224 10 288.94 14.71 0.00

TABLE 6 Summary of the four models obtained by combining the TABLE 7 Summary of the five models obtained by combining the most significant variables. Models are shown, degrees of freedom most significant variables of success in kleptoparasitic interactions (df), deviance, and significance level model (p-value) according to the studied variables. Degrees of freedom (df), deviance (Dev), and significance level model (p-value) Model df Deviance p 2 df Dev. res. df res. Dev χ θsex+Prey Size+Prey type+Landscape Prey type 2 14.339 .0008 Null 41 43.65 Sex 1 7.2637 .0070 Sex 1 0.05 40 43.60 0.83 Prey size 5 26.9652 <.0001 Age 2 0.23 38 43.37 0.89 Habitat 3 12.5862 .0056 Landscape 5 2.86 33 40.51 0.72 Habitat quality 1 0.03 32 40.48 0.88 θPrey size+Prey type+Landscape Prey type 2 14.339 .0008 Breeding status 1 0.02 31 40.461 0.89 Prey size 5 31.976 <.0001 Habitat 3 12.082 .007 In contrast, Sex, Prey size, Prey type, Landscape, and Technique showed significant results. θPrey type+Prey size Prey type 2 14.339 .0008 Based on the Akaike values and the deviance, we studied four new models (Tables 5 and 6). Prey size and Prey type are the variables that Prey size 5 31.976 <.0001 best explain hunting success, followed by Landscape and Sex, which θPrey size+Habitat quality only explained 7% of the variability. Using the parsimonious principle, Prey size 5 31.4722 <.0001 we can accept that the model takes into account prey characteristics Habitat 3 8.2713 .041 (Prey size and Prey type) and Landscape. In this sense, the most success occurs with reptiles (100% success) and prey of <50 gr (89% success). With respect to landscape characteristics, hunting success in closed 3.2 | Sexual differences in feeding behavior and areas was 35%, but increased until 50% in the remaining areas (open hunting techniques areas, dehesas). We identified the sex in 366 individuals. No intersexual differ- 2 ences were found in the techniques used by adults (χ = 0.32, 2 3.4 | Modelling kleptoparasitism interactions df = 3, p = .96) and juveniles (χ = 6.21, df = 3, p = .10, Table 2) but 2 we did find differences in subadults (χ = 14.87, df = 3, p = .002). Of the 57 individual kleptoparasitic interactions observed, 82.45% Subadult females used scavenging more frequently (40% vs. were successful. Sex, Age, Landscape, Habitat, or Breeding status af- 14.4%), whereas subadult males used hunting in flight more fre- fected the success of kleptoparasitic actions, but none of the variables quently (61.3% vs. 32%). were significant (Table 7).

3.3 | Modelling success in hunting in flight vs. from 4 | DISCUSSION a perch

Of the eight models examined (Tables 3 and 4), according to the Spanish imperial eagles, as in other raptor species including the

Akaike criteria, the best factor included the variable θSex, which indi- genus Aquila, use different attack techniques, with hunting from the cates that attack success is mainly influenced by the Sex of the individ- air and from perching sites being the most common techniques (see ual, with females being more successful than males (females: 58.9%; Cresswell & Quinn, 2010; Martínez et al., 2014; Quinn & Cresswell, males: 41.06%). Taking into account the deviance of the models, Prey 2004). However, our findings also show that kleptoparasitism and size and Prey type, together with Landscape, explain an important vari- scavenging are a regular feeding behavior, mainly in juvenile age- ability in hunting success. Table 4 shows how, among the eight vari- classes. Kleptoparasitism involves the opportunistic or habitual steal- ables considered, only three do not show significant results to explain ing of food items from other animals (Brockmanhn & Barnard, 1979). their influence on hunting success (Age, Habitat, and Breeding status). This results in fitness benefits for the kleptoparasite by saving time 6 | MARGALIDA et al. and effort (Brockmanhn & Barnard, 1979; Cresswell, 2004; Shealer, 1983 and 1985 as a consequence of the viral hemorrhagic disease Spendelow, Hatfield, & Nisbet, 2005). According to our results, (RHD), partially modifying the Spanish imperial eagle’s dietary habits Spanish imperial eagles increase their hunting success with age, with (Sánchez et al., 2009). scavenging and kleptoparasitic actions being important alternatives According to our model, prey characteristics and, to a lesser de- techniques to obtain food during the juvenile stage (first and second gree, landscape, determine the hunting success of Spanish imperial year). The inexperience of juvenile individuals obliges them to adopt eagles. This agrees with several studies that have shown that the these alternatives to obtain prey and save time and effort (Shealer hunting strategies, prey type, and prey vulnerability may also be fac- et al., 2005). However, some individuals seem to use scavenging tors determining hunting success (Cresswell & Quinn, 2004; Kenward, throughout their life regardless of habitat quality, suggesting that in- 2006; Cresswell, Lind, & Quinn, 2010). Our models show that sex is dividual personality also could influence this behavior (authors unpubl. not a relative good predictor (7%) of hunting success in Spanish im- data). These individuals can learn to handle these less valuable prey as perial eagles, which is similar to the results obtained in other studies alternative prey (Hughes, 1979), balancing the biomass provided by with golden eagles (Collopy, 1983), African peregrines Falco peregri- other prey, as well the time and energy invested to obtain them with nus minor (Jenkins, 2000) and Bonelli’s eagles Aquila fasciata (Martínez hunting techniques. et al., 2014). However, habitat quality and prey type and size are im- Several studies have shown that hunting success is higher in adults portant predictors. Thus, the openness of the habitat is a determining than in preadult individuals (Toland, 1986; Redpath, Amar, Madders, factor explaining hunting success for terrestrial prey, with the mainte- Leckie, & Thirgood, 2002; Kitowski, 2003). In the case of Spanish im- nance of open landscapes being an important management action to perial eagles, until individuals achieve enough experience, preadults improve hunting opportunities (Martínez et al., 2014; Ontiveros et al., use kleptoparasitism and scavenging to obtain food resources. The 2005). fact that none of the variables adequately explained the success of This approach shows the importance of direct observations to in- kleptoparasitic interactions suggests that this is an opportunistic be- crease our knowledge of individual behavioral traits that can contrib- havior that individuals use sporadically. With respect to the use of ute to improve management and conservation actions. For example, scavenging, the important frequency of carrion consumption is unex- with respect to the important role of scavenging on preadult individ- pected for a species with a diet mainly based on live prey (González, uals, this finding suggests that Spanish imperial eagles are also prone 1991; Sánchez et al., 2008), although methods to assess the diet to mortality related to the illegal use of poison baits, as occurs with could also influence biases in their determination. According to our other vulture species (Hernández & Margalida, 2008, 2009; Margalida results, the absence of a relationship to landscape variables, such as et al., 2014; Mateo-Tomás, Olea, Sánchez-Barbudo, & Mateo, 2012). habitat quality, suggests that scavenging behavior is independent of In fact, between 1990 and 2010, a total of 117 Spanish imperial eagles the abundance of live prey. In this sense, it should be noted that the were poisoned (Margalida, 2012), suggesting that this is a key factor estimates of habitat quality (i.e., density of rabbits) may not be com- for Spanish imperial eagle conservation (González, Margalida, Mañosa, pletely reliable due to methodological limitations (Fernández de Simón Sánchez, & Oria, 2007). A more recent threat related to scavenging et al., 2011). Moreover, prey abundance does not imply prey availabil- behavior is the ingestion of livestock carrion treated with diclofenac, ity (Ontiveros, Pleguezuelos, & Caro, 2005) nor is the proportion of a nonsteroidal anti-inflammatory drug (NSAID), which was the main prey consumed selected in proportion to its occurrence (Margalida, cause of vulture population declines in Asia (Green et al., 2004; Oaks Bertran, & Heredia, 2009). On the other hand, on several mamma- et al., 2004) and was authorized in Spain as of 2013 (Green, Donázar, lian carnivores have been suggested the switch between hunting and Sánchez-Zapata, & Margalida, 2016; Margalida et al., 2014). The po- scavenging based on seasonality in carrion supply and prey vulnerabil- tential threat to facultative raptors was evidenced by the mortality of ity to predation (Pereira, Owen-Smith, & Moleón, 2014). According to Steppe eagles Aquila nipalensis (Sharma et al., 2014) suggesting the our models, low prey density is not a driver of carrion use for preadult possibility that diclofenac is toxic to other accipitrid raptors, such as individuals, suggesting that poor hunting abilities obliges this age-class the threatened Spanish imperial eagle. (mainly juveniles) to use this alternative feeding behavior regularly. Although to our knowledge this is the first quantification of the im- ACKNOWLEDGMENTS portance of scavenging behavior in a larger eagle through direct observations, a similar result was indirectly observed in golden eagles in We thank C. Dávila, J. López, J. Caballero, L. Prada, M.J. Palacios, and a study with cameras and carrion provided experimentally. Golden ea- J. Caldera by their help during fieldwork. R. Finat and J.M. Tercero fa- gles appeared at 54% of the carrions observed (Sánchez-Zapata et al., cilitate the access to some private areas. The comments of two anony- 2010). In addition, although Spanish imperial eagle is generally consid- mous reviewers improved a previous version of this article. A.M. was ered to be specialized in the capture of rabbits (Ferrer & Negro, 2004), supported by a Ramón y Cajal research contract by the Ministry of recent studies detected an important variability in the diet spectrum Economy and Competitiveness (RYC-2012-11867). found between regions (Sánchez et al., 2009). This suggests that when the main prey (i.e., wild rabbit) is scarce, the Spanish imperial eagle’s CONFLICT OF INTERESTS diet is based on alternative prey, such as pigeons or carrion. These dietary shifts were probably accentuated after the rabbit crash between None declared. MARGALIDA et al. | 7

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