Joan Real

Demography and conservation of western European Bonelli's eagle Hieraaetus fasciatus populations

Abstract The basic demographic parameters of six Bonellis eagle Hieraaetus fasciatus populations in Spain and France were calculated from field data obtained in the last 15 years. Average annual productivity ranged from 0.36 to 1.24 young/pair and average annual adult survival from 84% to 96%. Preadult survival (from fledging to recruitment) was estimated at 10%. All the populations were declining at annual rates ranging from −7.3 to −1.1%. Although no statistically significant disagreement was observed between the predictions of a Leslie matrix model fitted to the population parameters and the real trends, some populations declined faster and others more slowly than expected. These differences were interpreted as a result of differential emigration, recruitment rates or preadult survival not accounted for by the model. Since the intrinsic population growth rate was about four times less sensitive to changes in preadult survival than to changes in adult survival, and about ten times less sensitive to changes in fecundity and predispersal survival, conservation efforts must be primarily directed towards increasing adult and preadult survival. Power line casualties and direct persecution must be eliminated in order to reduce mortality. Priorities on research should address dispersal, mortality and habitat relationships involving these two parameters. Monitoring should be extended to other populations.

Biases in diet study methods in the Bonelli's eagle

We compared 3 methods of studying diets of Bonellis eagle (Hieraaetus fasciatus): (1) recent prey present in the nest; (2) remains collected in the nest after breeding; and (3) pellet contents, with the delivered prey by the eagles in 2 nests. Remains collected after breeding was the only method that differed (P = 0.001) from delivered prey by underestimating small prey, especially red squirrel (Sciurus vulgaris) and ocellated lizard (Lacerta lepida), and overestimated pigeons (Columba spp). Study of prey consumption patterns showed that small prey frequently were fully consumed but remains were often left from medium and large prey. Rabbits (Oryctolagus cuniculus), the largest prey, appeared in similar proportions to those in which they were delivered, probably due to the fact that the eagles removed the largest bones from the nest. Although the recent-prey-present method did not show significant differences (P = 0.730) from delivered prey, the method could hide some biases linked to the greater probability of detecting large prey such as rabbits. Considering the accuracy and the effort involved in obtaining information, we conclude that pellet analysis is the most efficient method of monitoring the diet of Bonellis eagle.

From local monitoring to a broad-scale viability assessment: a case study for the Bonelli's Eagle in western Europe

Population viability analysis (PVA) has become a basic tool of current conservation practice. However, if not accounted for properly, the uncertainties inherent to PVA predictions can decrease the reliability of this type of analysis. In the present study, we performed a PVA of the whole western European population (France, Portugal, and Spain) of the endangered Bonellis Eagle (Aquila fasciata), in which we thoroughly explored the consequences of uncertainty in population processes and parameters on PVA predictions. First, we estimated key vital rates (survival, fertility, recruitment, and dispersal rates) using monitoring, ringing, and bibliographic data from the period 1990-2009 from 12 populations found throughout the studied geographic range. Second, we evaluated the uncertainty about model structure (i.e., the assumed processes that govern individual fates and population dynamics) by comparing the observed growth rates of the studied populations with model predictions for the same period. Third, using the model structures suggested in the previous step, we assessed the viability of both the local populations and the overall population. Finally, we analyzed the effects of model and parameter uncertainty on PVA predictions. Our results strongly support the idea that all local populations in western Europe belong to a single, spatially structured population operating as a source- sink system, whereby the populations in the south of the Iberian Peninsula act as sources and, thanks to dispersal, sustain all other local populations, which would otherwise decline. Predictions regarding population dynamics varied considerably, and models assuming more constrained dispersal predicted more pessimistic population trends than models assuming greater dispersal. Model predictions accounting for parameter uncertainty revealed a marked increase in the risk of population declines over the next 50 years. Sensitivity analyses indicated that adult and pre-adult survival are the chief vital rates regulating these populations, and thus, the conservation efforts aimed at improving these survival rates should be strengthened in order to guarantee the long-term viability of the European populations of this endangered species. Overall, the study provides a framework for the implementation of multi-site PVAs and highlights the importance of dispersal processes in shaping the population dynamics of long-lived birds distributed across heterogeneous landscapes.

TRICHOMONIASIS IN A BONELLI'S EAGLE POPULATION IN SPAIN

During 1980–97, trichomoniasis was detected in nestlings of Bonellis eagle Hieraaetus fasciatus in Catalonia (Spain). In 1993 Trichomonas gallinae was isolated in 36% of nestlings (n = 39) and affected 41% of broods (n = 22). Overall, trichomoniasis was one of the most important single nestling mortality factor, accounting for 22% of total chick mortality, and causing the death of 2% of chicks. Trichomoniasis deaths took place during the second half of the nestling period. The median age at death was 45.5 days. Although the presence of the parasite was not related to the composition of the diet or parental age, pairs that developed the disease ate more pigeons and included more often non-adult birds. At present trichomoniasis apparently has little demographic impact on the Bonellis eagle population in Catalonia, but the eventual spread of this disease in chicks and its unknown effects on adults might be of concern.

Modelling the risk of collision with power lines in Bonelli's Eagle Hieraaetus fasciatus and its conservation implications.

´´ Summary Power line casualties are considered one of the main causes of mortality in the endangered Bonelli’s Eagle Hieraaetus fasciatus, although little is known about factors involved in collisions with wires and their consequences at population level. We studied 18 radio-tracked individuals to determine the risk of collision with power lines at two spatial scales (flight height and span crossings). Through logistic regression modelling we found that the risk of collision was mainly determined by eagles’ home range use, being reduced in kernel 80%, kernel 95% and MCP respectively to 0.421, 0.114 and 0.032 times in comparison to risk associated to the 50% kernel area. In addition, the risk of collision increased in open habitats (around 1.5 times higher than in forested habitats) far from urban areas (2.345 times higher than near urban areas) that were good for hunting, and in cliff areas used for breeding and roosting, where eagles fly at a lower height (the probability of eagles flying at a low height was 1.470 times higher than in forested habitats). A significant positive correlation was found between territorial turnover rates and the risk ascribed to transmission lines with earth wires in 15 breeding territories. Moreover, this correlation had a higher significance for the 50% kernel area when transmission without earth wires and double circuit distribution lines were added, although no correlations were encountered for distribution lines. These results suggested that power line collisions might be more important than previously reported as a cause of mortality for the species and thus conservation actions should be applied in order to minimise their effects on population dynamics. Predictive models may be a useful tool in careful planning of new power line routes and the wire-marking of the existing ones. Kernel areas should be used rather than fixed radii given that distances from nests may not adequately match the risk of collision.

Quick methods for evaluating survival of age‐characterizable long‐lived territorial birds

ABSTRACT Survival is a key life-history trait in animals. However, most methods of survival estimation require substantial human and economic investment in the long term, particularly in species occurring in low densities, the case of most endangered species. An alternative to traditional recapture (CR) methods is estimation of adult survival based indirectly on either age ratios (AGR) or turnover rates (TOR) in territorial species. These 2 methods are applicable to bird species in which recruited individuals enter into the breeding population whilst still exhibiting the external traits that distinguish those animals from experienced adults. The main advantages of these methods are that survival can be easily estimated for all monitored individuals after just 1 or 2 breeding seasons and that disturbance to the species is minimized. The main constraints of indirect methods are that the assumptions are more restrictive than in CR methods, and survival estimates, although comparable between sites and years, may be biased. We used data from a long-term monitoring survey of 2 populations of the endangered Bonellis eagle (Aquila fasciata), one in Catalonia (NE Spain) and the other in Provence and Languedoc-Roussillon (SE France). We evaluated survival estimates using the AGR and TOR methods and compared them with CR methods and provide suitable corrections for refining survival estimates based on indirect methods. In Catalonia (2002–2008), survival was estimated at 0.84 by CR methods (SE = 0.047; n = 25 radio tagged eagles), at 0.86 by the corrected AGR method (SE = 0.011; n = 558 bird * year), and at 0.86 by the corrected TOR method (SE = 0.022; n = 547 bird * year). In France (1999–2008), survival was estimated at 0.88 by CR methods (SE = 0.040; n = 45 darvic banded eagles), at 0.87 by the corrected AGR method (SE = 0.015; n = 443 bird * year), and at 0.87 by the corrected TOR method (SE = 0.015; n = 438 bird * year). All analyses suggest that females survive better than males and that individuals from the French population survive better than individuals from the Catalan population. We conclude that indirect methods, which should not be regarded as a substitute of CR methods, will allow wildlife managers and researchers to estimate accurately adult survival in a territorial species over a short period of time and to monitor survival across populations over large geographic ranges and over time.

Multi-Scale Effects of Nestling Diet on Breeding Performance in a Terrestrial Top Predator Inferred from Stable Isotope Analysis

Inter-individual diet variation within populations is likely to have important ecological and evolutionary implications. The diet-fitness relationships at the individual level and the emerging population processes are, however, poorly understood for most avian predators inhabiting complex terrestrial ecosystems. In this study, we use an isotopic approach to assess the trophic ecology of nestlings in a long-lived raptor, the Bonelli’s eagle Aquila fasciata, and investigate whether nestling dietary breath and main prey consumption can affect the species’ reproductive performance at two spatial scales: territories within populations and populations over a large geographic area. At the territory level, those breeding pairs whose nestlings consumed similar diets to the overall population (i.e. moderate consumption of preferred prey, but complemented by alternative prey categories) or those disproportionally consuming preferred prey were more likely to fledge two chicks. An increase in the diet diversity, however, related negatively with productivity. The age and replacements of breeding pair members had also an influence on productivity, with more fledglings associated to adult pairs with few replacements, as expected in long-lived species. At the population level, mean productivity was higher in those population-years with lower dietary breadth and higher diet similarity among territories, which was related to an overall higher consumption of preferred prey. Thus, we revealed a correspondence in diet-fitness relationships at two spatial scales: territories and populations. We suggest that stable isotope analyses may be a powerful tool to monitor the diet of terrestrial avian predators on large spatio-temporal scales, which could serve to detect potential changes in the availability of those prey on which predators depend for breeding. We encourage ecologists and evolutionary and conservation biologists concerned with the multi-scale fitness consequences of inter-individual variation in resource use to employ similar stable isotope-based approaches, which can be successfully applied to complex ecosystems such as the Mediterranean.

Pollutant accumulation patterns in nestlings of an avian top predator: biochemical and metabolic effects

The exposure to persistent pollutants such as organochlorine compounds (OCs) or metals has been associated with declines in top predator populations, which can accumulate high amounts of these pollutants from their prey. However, understanding how variation in OC and metal accumulation in wild species affects their biochemical and physiological responses is a big challenge, especially for endangered predators like the Bonellis eagle (Aquila fasciata). This bird of prey is an interesting study model because the differences in diet composition among populations and territories can account for important pollutant uptake variations. We compared OC and metal accumulation in blood of Bonellis eagle nestlings from three populations across Spain as a function of origin, age class (nestlings vs. adults), sex and number of siblings per nest, and related accumulation patterns to responses indicative of body condition, biochemistry and antioxidant status. Nestlings from Catalonia, the most industrialized area, showed the highest concentrations of PCBs and arsenic, and the lowest concentrations of zinc. The two former substances, together with DDTs, exerted an overall influence on nestlings physiology. PCBs and arsenic were associated with reduced retinol levels, pointing to oxidative damage in exposed individuals, which was also consistent with the low zinc levels in individuals from the polluted region. Increased plasma DDT levels were related to reduced body condition and lower levels of triglycerides. Mercury accumulation in Castile and Leon was higher in nestlings that were alone in the nest than in nestlings that shared it with a sibling; this suggests an increased mercury uptake from secondary prey in territories where preferred prey (i.e. rabbits) are scarce, which are also the territories where productivity is reduced. Overall, the results reveal a spatial variation in pollutant accumulation patterns and associated physiological effects, and suggest the major role that territory quality may have in such patterns.

Retrofitting of power lines effectively reduces mortality by electrocution in large birds: an example with the endangered Bonelli's eagle

Summary 1. Mortality caused by power lines is a conservation problem for many vulnerable bird species. Many large species are especially threatened by electrocution as they frequently perch on pylons leading to electrocution that typically causes death. Electrocution mitigation measures have been implemented to protect several species; however, a resulting decrease in mortality due to these measures has not previously been demonstrated at the population scale. 2. In this study, we used data from a long-term capture–recapture programme (combining resightings of live birds and recovery of dead birds) carried out on the French population of the Bonelli’s eagle Aquila fasciata from 1990 to 2009 to estimate the impact of the insulation of power lines on key demographic rates. 3. We found that the survival probability of all age classes increased after the insulation of dangerous power lines, due to a decrease in mortality caused by electrocution. This decrease was partially compensated for by an increase in other causes of death. 4. Our findings show that insulation of power lines has a strong positive impact on juveniles and immature birds and a lesser impact on adults. The overall increase in survival due to power line insulation led to a sharp increase in predicted population growth rates (from 082 to 098), although our findings still suggest that the population is not self-sustaining. Elasticity values indicate that adult survival is the key parameter in the population dynamics of this species, and since adult mortality caused by electrocution seemed close to zero, our ability to act on this parameter is limited. 5. This study demonstrates that insulation of power lines is relevant for the conservation of large bird species at a population scale as it allows the survival rate of all age classes to increase and thus in turn has a strong positive impact on population growth rates. 6. Synthesis and applications. We demonstrated that mortality rates induced by electrocution are considerable and have major consequences for the population viability of birds. We also demonstrated that electrocution mitigation measures can lead to a sharp increase in survival through reducing mortality from electrocution leading to improved population viability. In the light of these results, there is an urgent need that conservationists contact power line stakeholders not only to urge them to generalize retrofitting actions but also, in planning new infrastructure development, to plan for less harmful power lines, since this will be far less costly than developing a posteriori mitigation actions.

Changes in intrapopulation resource use patterns of an endangered raptor in response to a disease‐mediated crash in prey abundance

1. A long-standing question in ecology is how natural populations respond to a changing environment. Emergent optimal foraging theory-based models for individual variation go beyond the population level and predict how its individuals would respond to disturbances that produce changes in resource availability. 2. Evaluating variations in resource use patterns at the intrapopulation level in wild populations under changing environmental conditions would allow to further advance in the research on foraging ecology and evolution by gaining a better idea of the underlying mechanisms explaining trophic diversity. 3. In this study, we use a large spatio-temporal scale data set (western continental Europe, 1968-2006) on the diet of Bonellis Eagle Aquila fasciata breeding pairs to analyse the predator trophic responses at the intrapopulation level to a prey population crash. In particular, we borrow metrics from studies on network structure and intrapopulation variation to understand how an emerging infectious disease [the rabbit haemorrhagic disease (RHD)] that caused the density of the eagles primary prey (rabbit Oryctolagus cuniculus) to dramatically drop across Europe impacted on resource use patterns of this endangered raptor. 4. Following the major RHD outbreak, substantial changes in Bonellis Eagles diet diversity and organisation patterns at the intrapopulation level took place. Dietary variation among breeding pairs was larger after than before the outbreak. Before RHD, there were no clusters of pairs with similar diets, but significant clustering emerged after RHD. Moreover, diets at the pair level presented a nested pattern before RHD, but not after. 5. Here, we reveal how intrapopulation patterns of resource use can quantitatively and qualitatively vary, given drastic changes in resource availability. 6. For the first time, we show that a pathogen of a prey species can indirectly impact the intrapopulation patterns of resource use of an endangered predator.