This paper discusses, for the first time, the patterns of occurrence of passerine species with feeding activity at experimental carrion inputs. It aims to reveal the factors that determine their presence and abundance depending on (1) the characteristics of the carrion, the surrounding landscape and spatiotemporal conditions, and (2) their relationship with other scavengers to analyze potential competitive interactions. Specifically, we tried to recognize the behavioral association between passerines and scavenger raptors regarding their simultaneous abundance at carcasses and the sequence of consumption since the carrion was supplied. Due to differences between corvids and non‐corvids in relation to their scavenging status, the two groups of passerines were considered separately in the analyses.

The passerines are the most species‐rich order of birds, which means that the group shows a high level of heterogeneity in foraging adaptations and requirements. Regarding carrion use, most passerine species are not scavengers except for the family Corvidae, in which common carrion consumption has been shown ( Soler and Soler 1991 , Read and Wilson 2004 ). The facultative scavenging nature of the corvids varies depending on the species and according to non‐exclusive factors such as the geographical scope, habitat characteristics, territorial behaviour, inter‐and intra‐specific competitive mechanisms, or the availability of carcasses (Heinrich 1988, Read and Wilson 2004 ). In some cases other non‐corvid passerines that are not considered scavengers are active participants in the process of carrion consumption ( Selva et al. 2005 ), exploiting the side‐effects of these pulsed resources, such as a higher concentration of scavenger invertebrates ( Melis et al. 2007 , Barton et al. 2013 ). However, no specific studies have addressed in detail the factors that determine the presence of (mainly non‐corvid) passerines at carcasses for feeding purposes.

Methods

Study area The study was carried out at six sites in the Iberian Peninsula (Spain), three in the northeast (Pyrenean mountains range) and three in central‐west (Sierra Morena, Montes de Toledo‐Sierra de San Pedro ranges; Fig. 1). These two Iberian regions, of varied climate, vegetation, altitude and land use, were selected so as to include a wide diversity of bird species, both scavengers and non‐scavengers, in the study (Del Moral and Martí 2003). The northeastern area is situated between the Mediterranean continental and the high‐altitude mountain climatic sub‐regions. Mean temperature in winter (January) is 2.9°C and in summer is 20.3°C (July). The altitude of the study locations ranged between 1045 and 1330 m asl. The vegetation of the surroundings was mainly formed by Pinus sylvestris forests, subalpine grasslands and a series of shrub‐tree developments. The main socioeconomic land‐uses are extensive grazing, ecotourism and, to a lesser extent, big game harvesting. The central‐western subregion has a continental Mediterranean climate with hot summers, with an altitude ranging between 521 and 686 m asl. Mean temperature in winter (January) is 5.7°C and in summer is 25.4°C (July). The prevailing vegetation corresponds to Quercus rotundifolia and Quercus suber accompanied by other typical Mediterranean species, shaped as pasturelands (dehesa) or as unmanaged forests, and grasslands. Big game hunting, logging activities mainly from cork exploitation and extensive grazing are the main incomes for the local population. Figure 1 Open in figure viewer PowerPoint Study area in the Iberian Peninsula (Spain). The locations (dots) where experimental carrion inputs were controlled are shown, within northeastern (1 = Tremp; 2 = Buseu; 3 = Alt Pirineu Natural Park) and central‐western (4 = Cabañeros National Park; 5 = Alcudia‐Sierra Madrona Natural Park; 6 = Sierra de San Pedro) sub‐regions. Experimental sites were selected on active supplementary feeding points maintained within the frame of official conservation programs to favor scavenger bird species. These points were choosen because a different type of management was carried out before the start of the essay (predictability variable; Table 1). The species of avian scavengers and forest passerines within the study area show relative abundances high enough to consider their presence at the supplementary feeding points as representative of the whole Iberian Peninsula. Thus, for vulture species, within the northeastern sub‐region an average of 347 pairs of Griffon Vulture Gyps fulvus, five of Cinereous Vulture Aegypius monachus, 18 of Egyptian Vulture Neophron percnopterus and 15 of Bearded Vulture Gypaetus barbatus were registered in a 25 km radius around the three locations of carrion inputs (R. Moreno‐Opo and A. Margalida, unpublished data). For the central‐western sub‐region the average numbers of breeding pairs of the species mentioned above in the three locations were, respectively, 90, 148, 7 and 0 (R. Moreno‐Opo and A. Margalida, unpublished data). Other bird species were not the subject of population estimates in our field work. Nonetheless, there is a widespread occurrence of different species typical of forest environments in the vicinity of the tested points (Del Moral and Martí 2003). Furthermore, according to distribution patterns of bird species richness based on environmental (habitat, weather, productivity), geographical and human characteristics (González‐Taboada et al. 2007, Moreno‐Rueda and Pizarro 2010), there should be a higher richness and relative abundance of birds in the central‐western subregion, in comparison to the northeastern one. Table 1. Independent variables regarding the characteristics of the provided carrion in experimental inputs, considered to assess their influence on the presence and relative abundance of passerine birds with feeding activity.

Study design and data collection Between May 2009 and April 2011 an experimental program of carrion inputs at supplementary feeding points for avian scavengers was performed. Carrion was supplied at each point every 15 days, controlling its characteristics and combining inputs sequentially (mainly format and scattering variables; Table 1). In addition, other carrion remains were provided within the schedule of the management program of the supplementary feeding sites. These were not monitored but considered ahead regarding its possible influence on the attendance of birds to the experimental sites (predictability variable; Table 1). Thus, at the end of the two‐year experiment, a similar number of inputs with each of the combinations of the studied variables was implemented. The provided carrion consisted of cadavers and remains of livestock, mainly Sheep Ovis aries, and wild ungulates such as Red Deer Cervus elaphus and Wild Boar Sus scrofa. The management of the animal by‐products was developed in accordance with current sanitary legislation (European Commission 2011). Carrion exploitation was continuously recorded from the time of its provision until three days later, during the daytime from sunrise to sunset. For this purpose, we installed a high‐resolution videocamera (Arecont Vision Megavideo AV5100) connected to a computer, hard disk drive and rechargeable lithium batteries. The camera was located within 20 m from the point of supply, allowing the observation of a wide area around the carrion due to the 120° display angle of the camera. The recording quality was controlled, so that images occurred in a sequence of 20 frames per second with a resolution of 5 megapixels. This high resolution allowed zoom images to capture accurate data on the studied variables (see sections below). Images were stored on the hard disk drive for subsequent visualization and study, through the AV program v.5.1.4.239 Application Manager (Arecont Vision, Glendale, California, USA).

Response and explanatory variables The recordings of each three‐day event of carrion consumption were visualized by registering different independent and response variables. The first were addressed to determine the number of passerines showing feeding activity. Thus, the following were considered: (1) bird counts in each 10‐min period (i.e., every 10 min a census of the birds was carried out); and (2) the total number of birds that visited the carrion after each input, expressed as the sum of birds recorded in the different 10‐min periods. Passerines were identified to the species level, although some small‐sized species had to be assigned to their genus or families. The following were selected as independent variables, depending on the analysis performed: (1) the number of individuals of scavenger raptors present (Griffon Vulture, Cinereous Vulture, Bearded Vulture, Egyptian Vulture, Black Kite Milvus migrans, Red Kite Milvus milvus, Spanish Imperial Eagle Aquila adalberti, Golden Eagle Aquila chrysaetos, Common Buzzard Buteo buteo and Montagu's Harrier Circus pygargus) recorded using the same procedure as passerines; (2) the number of hours since the provision; and (3) carrion characteristics and space‐time circumstances (Table 1). For the purposes of this study, it was considered as obligate scavengers those individuals of vulture species, as facultative scavengers other raptors different to vultures and passerines of the Corvidae family, and as non scavengers passerines not belonging to the Corvidae family. The numerical relationships between occurrence of passerines (we also observed, and so included in this category, two non passerine species the Hoopoe Upupa epops and Wood Pigeon Columba palumbus) and raptors feeding on carrion were first analyzed, to evaluate possible exclusion‐competition‐facilitation mechanisms that could occur between the two groups. To this end, this relationship was assessed in each 10‐min period in which individuals of any of the two groups (passerines and/or scavenger raptors) were present. Pseudoreplication between subsequent counts of 10 min that could lead to the lack of independence of the observations was discarded. Based on the analysis and data gathering from the images, it was observed that the permanence of individuals was dynamic and continuously changing (Cortés‐Avizanda et al. 2010). In fact, in most cases, the residence time of individuals was less than 10 min, especially for passerines (personal observations). Due to the large distances between sampling points within the same study sub‐regions and to the weekly interval between inputs at different points, spatial autocorrelation therein was dismissed. Furthermore, the temporal progress of attendance of passerines to the carcasses was assessed with the objective of recognizing possible excluding relationships between species. This was obtained by calculating the mean number of birds counted from the time of the input at 0.1 h intervals. In addition, the influences of different variables (Table 1) on the total number of passerines that came to each input—as the sum of the birds recorded in the different 10‐min periods—were analyzed. These variables were selected in order to elucidate possible effects related to the study area, the time of year, the management performed at the supplementary feeding point or the carrion characteristics. In all cases corvids, whose opportunistic and facultative scavenging behavior is common (Soler and Soler 1991, Heinrich 1998), and other passerine species not considered scavengers were analyzed separately.