Study areas and fieldwork. The five species of diurnal and nocturnal raptors used in this study were the goshawk (Accipiter gentilis), pygmy owl (Glaucidium passerinum), Tengmalm’s owl (Aegolius funereus), tawny owl (Strix aluco) and scops owl (Otus scops). The diet of these species consists mainly of medium-sized birds and mammals (for goshawk and pygmy owl), small mammals and birds (Tengmalm’s owl), small mammals (tawny owl), and arthropods and small vertebrates (scops owl). In our region (Supplementary Figure 1), the main breeding habitat is mature forests for goshawks, Tengmalm’s owls and pygmy owls, younger woodland managed by stool-shoot regeneration (coppice) for tawny owls, and grassland for scops owls. Therefore, these species span a wide range of diel activity patterns (diurnal or nocturnal), habitat associations and resource use. Each raptor species was surveyed in a different plot of the central-eastern Italian Alps (Supplementary Figure 1). The territories of all species were already known at the beginning of this study as part of an investigation of the whole alpine raptor community e.g.1,2,3,4 (included in Project Biodiversità, funded by the Autonomous Province of Trento). In particular, goshawks were surveyed in a 700 km2 plot (containing 25 territories), Tengmalm’s owls in a 553 km2 plot (31 territories), pygmy owls in a 539 km2 plot (32 territories), tawny owls in a 55 km2 plot (33 territories), and scops owls in a 50 km2 plot (40 territories).
We used the diversity of birds as a surrogate of biodiversity. For grassland sites (i.e. those occupied by scops owls and their associated spatial and taxonomic controls), we also assessed the diversity of butterfly species (Rhopalocera). These taxa are commonly used for biodiversity assessment because of their visibility, ease of census and positive relationship with the diversity of other taxa5,6. We censused birds by song-recognition during point-counts and butterflies by capturing all those seen within 10 m of a rectilinear 20 m transect (i.e. in a 20 x 20 m quadrat). Each point-count was conducted in May and repeated in June, during the first four hours after sunrise. At each site, we conducted a 10-min point-count, and then slowly walked 500 m towards the four main cardinal directions, noting all bird species not previously recorded. Therefore, each assessment reflected the biodiversity of an area of approximately 1 km2. To provide a further estimate of biodiversity less linked, in a trophic-sense, to the raptor species, we also recorded the number of tree species observed during each point-count.
The biodiversity assessments were conducted in 2002-2003 for Tengmalm’s owls (15 breeding sites in 2002, 10 breeding sites in 2003), in 2003 for scops owls and in 2004 for the other three species. To avoid the potentially confounding effects of yearly or seasonal variations in biodiversity levels, each control site was always matched with a raptor site in the following manner: if a raptor nest was sampled in day x of year y, its associated control sites (spatial control, taxonomic control site A and B and their own associated spatial controls, see below) were also sampled in day x or x+1 of the same year.
Statistical and GIS analyses. To test whether sites occupied by raptors for breeding were consistently associated with high biodiversity levels, we compared such sites with two types of control sites: (1) sites randomly selected within each study area (spatial-control sites), and (2) nests of randomly selected species of lower-trophic-levels (taxonomic-control sites A). The latter procedure may result in a set of abundant-generalist species, which may be poor biodiversity-indicators. Therefore, we provided a complementary test by locating the nests of another set of five lower-trophic-level species which were less abundant, more endangered, and with more specialized ecological requirements (taxonomic-control sites B). The comparison with spatial-controls tests whether the occurrence of top predators may be used to detect biodiversity hotspots, while the comparison with taxonomic-controls tests whether top predators may be more efficient biodiversity indicators than other species. In all tests, we randomly selected 25 nest-sites for each raptor species, and compared their biodiversity levels with those of 25 spatial-controls, 25 taxonomic-controls A, and 25 taxonomic-controls B. Spatial-control sites were selected in the following way, so as to control for the potentially confounding effect of habitat: for each raptor nest x in study area y, we selected a spatial-control: (1) located within y; (2) at the same elevation as x; (3) in the same vegetation type as x; (4) at a similar distance to habitat edges as x; (5) farther than 1 km from any other site (to avoid spatial autocorrelation); and (6) in a patch with a vegetation structure judged similar to x (e.g. if a raptor-site was located in a mature, multi-layered forest with three strata, the spatial-control was located in a forest with similar characteristics). Spatial-controls were originally plotted, imposing conditions 1-5 above, by means of the extension “Animal Movement” of the GIS software ArcView 3.2. If condition 6 did not hold during ground-surveys, the process was repeated until a suitable site was found. Taxonomic-control sites A were chosen in the following manner: for a raptor species in study area y, we: (1) listed all species of lower-trophic-levels known to occupy the same habitat type; (2) randomly selected one of them; (3) plotted 25 random locations within y; (4) visited each one and found the nearest nest of the selected species. The taxonomic-control A species were the robin (Erithaculus rubecula), blackbird (Turdus merula), blackcap (Sylvia atricapilla), crested tit (Parus cristatus) and chaffinch (Fringilla coelebs). We selected as taxonomic-control species B the hazel grouse (Bonasa bonasia), European nightjar (Caprimulgus europaeus), green woodpecker (Picus viridis), grey-headed woodpecker (Picus canus), and Eurasian treecreeper (Certhia familiaris), and censused 25 nests of each species in the same manner as for taxonomic-controls A. Finally, for each taxonomic-control, we plotted a spatial-control site (same procedure as above) to test whether such lower-trophic-level species could be employed as biodiversity-indicators.
Furthermore, for each type of location (predator-site, spatial-control, or taxonomic-control), we conducted a coarse gap analysis7,8. For each group of 25 sites, we: (1) selected the site with the highest species richness; and (2) progressively added sites with sets of species most complementary to the already selected one(s), until all species were represented in a hypothetical reserve-network.
Comparisons between raptor-sites and spatial- or taxonomic-controls were performed by means of t-tests with a Bonferroni correction for multiple comparisons. For each sampled-site, biodiversity was expressed as the total numbers of all species, the numbers of avian species classified as vulnerable (SPEC 1-49), the Shannon-Weaner diversity index calculated on all avian species10, or calculated on vulnerable species only. In each comparison, we excluded from biodiversity estimates the species that was the subject of the test.
Sergio, F., Marchesi, L. & Pedrini, P. Spatial refugia and the coexistence of a diurnal raptor with its intraguild owl predator. J. Anim. Ecol. 72, 232-245 (2003).
Sergio, F. & Penteriani, V. Public information and territory establishment in a loosely colonial raptor. Ecology86, 340-346 (2005).
Sergio, F., Marchesi, L., Pedrini, P., Ferrer, M. & Penteriani, V. Electrocution alters the distribution and density of a top predator, the eagle owl Bubo bubo. J. Applied Ecol. 41, 836-845 (2004).
Sergio, F., Scandolara, C., Marchesi, L., Pedrini, P. & Penteriani, V. Effect of agro-forestry and landscape changes on common buzzards (Buteo buteo) in the Alps. Animal Conservation7, 17-25 (2005).
Norris, K. and Pain, D. J. (eds.) Conserving Bird Biodiversity: General Principles and their Application (Cambridge University Press, Cambridge, 2002).
Gaston, K. J. (ed.) Biodiversity: a Biology of Numbers and Difference (Blackwell Science, Oxford, 1996).
Kerr, J. T. Species richness, endemism, and the choice of protected areas for conservation. Cons. Biol. 11, 1094-1100 (1997).
Jeggins, M. D. Gap analysis: concepts, methods and recent results. Landscape Ecol. 15, 5-20 (2000).
Tucker, G. M. & Heath, M. F. (eds.) Birds in Europe: their Conservation Status (BirdLife International, Cambridge, 1994).
Krebs, C. J. Ecological Methodology (HarperCollins, New York, 1998).