Role of prey and intraspecific density dependence on the population growth of an avian top predator

Exploring predator–prey systems in diverse ecosystems increases our knowledge about ecological processes. Predator population growth may be positive when conspecific density is low but predators also need areas with prey availability, associated with competition, which increases the risk of suffering losses but stabilises populations. We studied relationships between European rabbits Oryctolagus cuniculus (prey) and adult eagle owls Bubo bubo (predators) in south-western Europe. We assessed models explaining the predator population growth and stability. We estimated the abundance of rabbits and adult eagle owls during three years in eight localities of central-southern Spain. We explored models including rabbit and adult eagle owl abundance, accounting for yearly variations and including the locality as a random variable. We found that population growth of adult eagle owls was positive in situations with low conspecific abundance and tended to be negative but approaching equilibrium in situations of higher conspecific abundance. Population growth was also positively related to previous summer rabbit density when taking into account eagle owl conspecific abundance, possibly indicating that rabbits may support recruitment. Furthermore, abundance stability of adult eagle owls was positively related to previous winter–spring rabbit density, which could suggest predator population stabilisation through quick territory occupation in high-quality areas. These results exemplify the trade-off between prey availability and abundance of adult predators related to population growth and abundance stability in the eagle owl–rabbit system in south-western Europe. Despite rabbits have greatly declined during the last decades and eagle owls locally specialise on them, eagle owls currently have a favourable conservation status. As eagle owls are the only nocturnal raptor with such dependence on rabbits, this could point out that predators may overcome prey decreases in areas with favourable climate and prey in the absence of superior competitors with similar foraging mode.     

Evaluating the influence of diet-related variables on breeding performance and home range behaviour of a top predator

Diet composition is linked to reproductive performance directly or indirectly by other life-history traits, including home range behaviour. The relationships between prey abundance, diet and individual fitness have often been explored. However, these relationships are complex and difficult to disentangle, especially in vertebrate top predators. Here, we present the results of a long-term study using multi-model inference procedures to elucidate the influence of diet-related variables on breeding parameters and home range behaviour of a top predator, the eagle owl Bubo bubo. Superpredation, diet diversity, rat biomass and rabbit mean weight were the most important variables when analysing reproductive parameters, suggesting that less diverse diets with greater rabbit biomass percentage may benefit reproductive performance, whereas rat biomass percentage is apparently associated with greater variation of breeding success. Earlier laying dates seem to be associated with the consumption, on average, of smaller rabbits. On the other hand, edge density was the most relevant factor determining the variation in home range behaviour, with individual characteristics, such as age and sex, also being important. Although the relative importance of the diet-related variables was generally low, mean weight of alternative prey, diet diversity and rabbit biomass also helped to explain home range parameters. In an optimal foraging context, centred on the abundance of the main prey species, our results suggest that when rabbits are less available eagle owls may increase home range size in order to obtain alternative prey, increasing at the same time their dietary diversity, which may also require higher movement speed.     

Tawny owl vocal activity is constrained by predation risk

The vocal behaviour of birds may be influenced by many factors, including the risk of being detected by a predator. In Doñana Protected Area, the tawny owl co‐exists alongside its intraguild predator, the eagle owl Bubo bubo. We considered four scenarios to study the vocal behaviour of tawny owls at dusk by analysing: A) the calling rate of all males in 29 sites; B) the calling rate at dusk of males living within the home range of the intraguild predator; C) the calling rate of males living within the home range of the intraguild predator between 60 and 90 min after sunset; and D) the duration of male vocal bouts in visits where eagle owls have called. In scenario A we found that only the number of conspecific males affected the calling rate of tawny owls. In scenario B we observed that the presence of an eagle owl calling constrained the calling rate of the intraguild prey. In scenario C we found that this effect seemed mostly associated to a contemporaneous detection of the intraguild predator’s calls. Finally, in scenario D we found no significant effects on bout duration. These results seem to indicate that tawny owls use their intraguild predator’s calls as a cue to assess predation risk, and then adjust their vocal behaviour in order to minimize predation risk by a predator that may locate its prey by its vocalizations.     

Predator–prey relationships in a Mediterranean vertebrate system: Bonelli’s eagles,rabbits and partridges

How predators impact on prey population dynamics is still an unsolved issue for most wild predator–prey communities. When considering vertebrates, important concerns constrain a comprehensive understanding of the functioning of predator–prey relationships worldwide; e.g. studies simultaneously quantifying ‘functional’ and ‘numerical responses’ (i.e., the ‘total response’) are rare. The functional, the numerical, and the resulting total response (i.e., how the predator per capita intake, the population of predators and the total of prey eaten by the total predators vary with prey densities) are fundamental as they reveal the predator’s ability to regulate prey population dynamics. Here, we used a multi-spatio-temporal scale approach to simultaneously explore the functional and numerical responses of a territorial predator (Bonelli’s eagle Hieraaetus fasciatus) to its two main prey species (the rabbit Oryctolagus cuniculus and the red-legged partridge Alectoris rufa) during the breeding period in a Mediterranean system of south Spain. Bonelli’s eagle responded functionally, but not numerically, to rabbit/partridge density changes. Type II, non-regulatory, functional responses (typical of specialist predators) offered the best fitting models for both prey. In the absence of a numerical response, Bonelli’s eagle role as a regulating factor of rabbit and partridge populations seems to be weak in our study area. Simple (prey density-dependent) functional response models may well describe the short-term variation in a territorial predator’s consumption rate in complex ecosystems.     

The Young,the Weak and the Sick: Evidence of Natural Selection by Predation

It is assumed that predators mainly prey on substandard individuals, but even though some studies partially support this idea, evidence with large sample sizes, exhaustive analysis of prey and robust analysis is lacking. We gathered data from a culling program of yellow-legged gulls killed by two methods: by the use of raptors or by shooting at random. We compared both data sets to assess whether birds of prey killed randomly or by relying on specific individual features of the prey. We carried out a meticulous post-mortem examination of individuals, and analysing multiple prey characteristics simultaneously we show that raptors did not hunt randomly, but rather preferentially predate on juveniles, sick gulls, and individuals with poor muscle condition. Strikingly, gulls with an unusually good muscle condition were also predated more than expected, supporting the mass-dependent predation risk theory. This article provides a reliable example of how natural selection may operate in the wild and proves that predators mainly prey on substandard individuals.     

Rabbit (Oryctolagus cuniculus) abundance and protected areas in central-southern Spain: why they do not match?

European rabbits (Oryctolagus cuniculus), a keystone species in the Iberian Mediterranean ecosystem, are the staple prey of the Iberian lynx (Lynx pardinus) and the Spanish imperial eagle (Aquila adalberti). These predators require medium to high rabbit densities and a low degree of human disturbance. We compared rabbit abundances in areas of central-southern Spain under three levels of protection and management: protected areas, intensively managed (nonprotected) hunting estates, and other nonprotected areas. We used pellet abundance indices to estimate rabbit density in 118 surveys conducted during the summers of 2002 and 2003. We observed greater rabbit abundance in intensively managed hunting estates compared to protected areas and other nonprotected areas, perhaps because policy makers did not consider rabbit numbers when selecting priority areas. Alternatively, differences in game management practices (e.g., predator control or habitat management) may explain the higher rabbit densities observed in managed hunting estates. Our results suggest that the best feeding conditions for the Iberian lynx and the Spanish imperial eagle occur in intensively managed hunting areas, where such predators are frequently persecuted. The conservation of these endangered predators may require efforts to increase rabbit densities in protected areas.     

Avian top predator and the landscape of fear: responses of mammalian mesopredators to risk imposed by the golden eagle

Top predators may induce extensive cascading effects on lower trophic levels, for example, through intraguild predation (IGP). The impacts of both mammalian and avian top predators on species of the same class have been extensively studied, but the effects of the latter upon mammalian mesopredators are not yet as well known. We examined the impact of the predation risk imposed by a large avian predator, the golden eagle (Aquila chrysaetos, L.), on its potential mammalian mesopredator prey, the red fox (Vulpes vulpes, L.), and the pine marten (Martes martes, L.). The study combined 23 years of countrywide data from nesting records of eagles and wildlife track counts of mesopredators in Finland, northern Europe. The predation risk of the golden eagle was modeled as a function of territory density, density of fledglings produced, and distance to nearest active eagle territory, with the expectation that a high predation risk would reduce the abundances of smaller sized pine martens in particular. Red foxes appeared not to suffer from eagle predation, being in fact most numerous close to eagle nests and in areas with more eagle territories. This is likely due to similar prey preferences of the two predators and the larger size of foxes enabling them to escape eagle predation risk. Somewhat contrary to our prediction, the abundance of pine martens increased from low to intermediate territory density and at close proximity to eagle nests, possibly because of similar habitat preferences of martens and eagles. We found a slightly decreasing trend of marten abundance at high territory density, which could indicate that the response in marten populations is dependent on eagle density. However, more research is needed to better establish whether mesopredators are intimidated or predated by golden eagles, and whether such effects could in turn cascade to lower trophic levels, benefitting herbivorous species.     

Responses of naïve and experienced European rabbits to predator odour

The response of prey species to predator scent has been investigated in many mammalian species; however, there is little information about the responses of European wild rabbits at the population level. Therefore, we conducted a simple experiment to investigate the behavioural response of a rabbit population to native predator cues in the wild. We compared the response to the scent of a predator (red fox) in a wild rabbit population bred in semi-natural conditions and naïve to terrestrial predators with the response of a population in a similar environment where terrestrial predators were present. The response to predators was based on rabbit abundance, inferred from pellet counts and measured by the defecation rate per day (DRD). Our results indicate that rabbits responded to the odour of fox faeces in the treatment warrens, resulting in a lower DRD. The main anti-predator behaviour observed was spatial avoidance (warren abandonment), which seemed to be more accentuated for rabbits who had not previously had contact with foxes in the plot where terrestrial predators were excluded. In both the fenced and the unfenced plot, the differences in the effect of the predator odour between the control and treatment warrens disappeared after cessation of treatment, suggesting a flexible and adaptive behaviour of rabbits to predator cues.

     

Activity patterns at the Arctic Circle: nocturnal eagle owls and interspecific interactions during continuous midsummer daylight

Circadian rhythms result from adaptations to biotic and abiotic environmental conditions that cycle through the day, such as light, temperature, or temporal overlap between interacting species. At high latitudes, close to or beyond the polar circles, uninterrupted midsummer daylight may pose a challenge to the circadian rhythms of otherwise nocturnal species, such as eagle owls Bubo bubo. By non‐invasive field methods, we studied eagle owl activity in light of their interactions with their main prey the water vole Arvicola amphibius, and their competitor the white‐tailed eagle Haliaeetus albicilla during continuous midsummer daylight on open, treeless islands in coastal northern Norway. We evaluated circadian rhythms, temporal overlap, exposure, and spatial distribution. The owls maintained a nocturnal activity pattern, possibly because slightly dimmer light around midnight offered favourable hunting conditions. The eagles were active throughout the 24‐h period as opposed to the strictly diurnal rhythm reported elsewhere, thus increasing temporal overlap and the potential for interference competition between the two avian predators. This may indicate an asymmetry, with the owls facing the highest cost of interference competition. The presence of eagles combined with constant daylight in this open landscape may make the owls vulnerable to interspecific aggression, and contrary to the available literature, eagle owls rarely exposed themselves visually during territorial calls, possibly to avoid detection by eagles. We found indications of spatial segregation between owls and eagles reflecting differences in main prey, possibly in combination with habitat‐mediated avoidance. Eagle owl vocal activity peaked in the evening before a nocturnal peak in visual observations, when owls were active hunting, consistent with the hypothesis of a dusk chorus in nocturnal bird species. The owls may have had to trade‐off between calling and foraging during the few hours around midnight when slightly dimmer light reduced the detection risk while also providing better hunting conditions     

To dare or not to dare? Risk management by owls in a predator–prey foraging game

In a foraging game, predators must catch elusive prey while avoiding injury. Predators manage their hunting success with behavioral tools such as habitat selection, time allocation, and perhaps daring—the willingness to risk injury to increase hunting success. A predator’s level of daring should be state dependent: the hungrier it is, the more it should be willing to risk injury to better capture prey. We ask, in a foraging game, will a hungry predator be more willing to risk injury while hunting? We performed an experiment in an outdoor vivarium in which barn owls (Tyto alba) were allowed to hunt Allenby’s gerbils (Gerbillus andersoni allenbyi) from a choice of safe and risky patches. Owls were either well fed or hungry, representing the high and low state, respectively. We quantified the owls’ patch use behavior. We predicted that hungry owls would be more daring and allocate more time to the risky patches. Owls preferred to hunt in the safe patches. This indicates that owls manage risk of injury by avoiding the risky patches. Hungry owls doubled their attacks on gerbils, but directed the added effort mostly toward the safe patch and the safer, open areas in the risky patch. Thus, owls dared by performing a risky action—the attack maneuver—more times, but only in the safest places—the open areas. We conclude that daring can be used to manage risk of injury and owls implement it strategically, in ways we did not foresee, to minimize risk of injury while maximizing hunting success.     

Taphonomic study of leporid remains accumulated by the Spanish Imperial Eagle (Aquila adalberti)

Distinguishing leporid bones accumulated by different agents such as diurnal raptors, owls, mammals and humans is essential to gain an understanding of not only human subsistence activities but also past ecology. This is particularly relevant in Iberian Palaeolithic sites where leporid remains usually constitute the most abundant taxon. Among diurnal raptors the Spanish Imperial eagle (Aquila adalberti) has been one of the most important leporid predators throughout the Iberian Peninsula. In order to investigate the taphonomic signature of this raptor, rabbit remains from 79 pellets were examined. Results show a high proportion of distal elements of the limb bones and skull. Compared with other diurnal birds of prey, the assemblages produced by this species appear to show a higher degree of breakage and corrosion from digestion. These results place this predator within a category similar to the small mammal carnivores (category 5) in terms of skeletal element abundance, breakage and digestion. It is hoped that these data will enable analysts to identify leporid fossils accumulated by the Spanish Imperial Eagle in archaeological assemblages.     

Induced changes in island fox (Urocyon littoralis) activity do not mitigate the extinction threat posed by a novel predator

Prey response to novel predators influences the impacts on prey populations of introduced predators, bio-control efforts, and predator range expansion. Predicting the impacts of novel predators on native prey requires an understanding of both predator avoidance strategies and their potential to reduce predation risk. We examine the response of island foxes (Urocyon littoralis) to invasion by golden eagles (Aquila chrysaetos). Foxes reduced daytime activity and increased night time activity relative to eagle-na?ve foxes. Individual foxes reverted toward diurnal tendencies following eagle removal efforts. We quantified the potential population impact of reduced diurnality by modeling island fox population dynamics. Our model predicted an annual population decline similar to what was observed following golden eagle invasion and predicted that the observed 11% reduction in daytime activity would not reduce predation risk sufficiently to reduce extinction risk. The limited effect of this behaviorally plastic predator avoidance strategy highlights the importance of linking behavioral change to population dynamics for predicting the impact of novel predators on resident prey populations.     

Movement and direction of movement of a simulated prey affect the success rate in barn owl Tyto alba attack

The present study was aimed at testing a novel idea, that rather than maximizing their distance from a predator during close-distance encounters, prey species are better off moving directly or diagonally toward the predator in order to increase the relative speed and confine the attack to a single available clashing point. We used two tamed barn owls Tyto alba to measure the rate of attack success in relation to the direction of prey movement. A dead mouse or chick was used to simulate the prey, pulled to various directions by means of a transparent string during the owl's attack. Both owls showed a high success rate in catching stationary compared with moving food items (90% and 21%, respectively). Success was higher when the prey moved directly away, rather than towards the owls (50% and 18%, respectively). Strikingly, these owls had 0% success in catching food items that were pulled sideways. This failure to catch prey that move sideways may reflect constraints in postural head movements in aerial raptors that cannot move the eyes but rather move the entire head in tracking prey. So far there is no evidence that defensive behavior in terrestrial prey species takes advantage of the above escape directions to lower rates of predator success. However, birds seem to adjust their defensive tactics in the vertical domain by taking-off at a steep angle, thus moving diagonally toward the direction of an approaching aerial predator. These preliminary findings warrant further studies in barn owls and other predators, in both field and laboratory settings, to uncover fine predator head movements during hunting, the corresponding defensive behavior of the prey, and the adaptive significance of these behaviors.     

A new method for immunologically marking prey and its use in predation studies

We introduce a new method for immunologically examining predator gut contents. It differs from previously described gut content analyses because it does not require the development of prey-specific antibody probes. Instead, insect prey were marked with a readily available antigen, rabbit immunoglobulin G (IgG). We then assayed predators that had fed on IgG labeled prey with an enzyme-linked immunosorbent assay (ELISA) using goat anti-rabbit IgG. Of the predator species that fed on the IgG labeled prey, 98.8% of those with chewing mouthparts scored positive for IgG 1 h after feeding. Our prey-labeling ELISA was less efficient for detecting IgG prey remains in predators with piercing/sucking mouthparts. Only 29.5% of these individuals scored positive for rabbit IgG in their guts 1 h after feeding. An additional study was conducted to measure the retention time of IgG-labeled prey in the guts of two species of predators with chewing mouthparts. Results from this experiment showed that the retention time varied depending on the predator and prey species examined. Results from these studies indicate that this marking technique could have widespread use for analyzing the gut contents of predators with chewing mouthparts, but it has limited application for those predators with piercing/sucking mouthparts. This article presents the results of research only. Mention of a proprietary product does not constitute an endorsement or recommendation for its use by the USDA.     

Inferring Predator Behavior from Attack Rates on Prey-Replicas That Differ in Conspicuousness

Behavioral ecologists and evolutionary biologists have long studied how predators respond to prey items novel in color and pattern. Because a predatory response is influenced by both the predator’s ability to detect the prey and a post-detection behavioral response, variation among prey types in conspicuousness may confound inference about post-prey-detection predator behavior. That is, a relatively high attack rate on a given prey type may result primarily from enhanced conspicuousness and not predators’ direct preference for that prey. Few studies, however, account for such variation in conspicuousness. In a field experiment, we measured predation rates on clay replicas of two aposematic forms of the poison dart frog Dendrobates pumilio, one novel and one familiar, and two cryptic controls. To ask whether predators prefer or avoid a novel aposematic prey form independently of conspicuousness differences among replicas, we first modeled the visual system of a typical avian predator. Then, we used this model to estimate replica contrast against a leaf litter background to test whether variation in contrast alone could explain variation in predator attack rate. We found that absolute predation rates did not differ among color forms. Predation rates relative to conspicuousness did, however, deviate significantly from expectation, suggesting that predators do make post-detection decisions to avoid or attack a given prey type. The direction of this deviation from expectation, though, depended on assumptions we made about how avian predators discriminate objects from the visual background. Our results show that it is important to account for prey conspicuousness when investigating predator behavior and also that existing models of predator visual systems need to be refined.     

The importance of visual cues for nocturnal species: eagle owls signal by badge brightness

Nocturnal species may communicate by visual signals more frequentlythan previously thought. In fact, such species are habituallyactive around sunset and sunrise, when light conditions arestill suitable for visual communication. We investigated thecommunication function of a visual cue in the eagle owl Bubobubo, a nocturnal predator. In this species, territorial andcourtship displays peak during the sunset and sunrise periodsand involve the display of a white badge located on the throatwhose reflectance properties are sex and period dependent. Experimentalintrusions were conducted at 30 eagle owl territories in orderto understand the function of the white badge during contests.We analyzed the reactions of both male and female owners towarda taxidermic mount with a normal brightness and a brightness-reducedwhite badge, with both male and female territorial calls. Ourresults indicate that the white badge of eagle owls plays animportant role in visual communication during contests. Malesdisplayed more frequently toward male low-brightness mounts,which were also approached more closely or attacked. Femalebehavior did not differ between experimental groups. Furthermore,a positive relationship between male badge brightness and breedingoutput suggested a potential role of the white badge as an honestsignal of male quality. The need to convey information by visualcommunication in a nocturnal species may have promoted the evolutionof visual signals employed at crepuscule.     

Laying the foundations for a human-predator conflict solution: assessing the impact of Bonelli's eagle on rabbits and partridges

Background

Predation may potentially lead to negative effects on both prey (directly via predators) and predators (indirectly via human persecution). Predation pressure studies are, therefore, of major interest in the fields of theoretical knowledge and conservation of prey or predator species, with wide ramifications and profound implications in human-wildlife conflicts. However, detailed works on this issue in highly valuable –in conservation terms– Mediterranean ecosystems are virtually absent. This paper explores the predator-hunting conflict by examining a paradigmatic, Mediterranean-wide (endangered) predator-two prey (small game) system.

Methodology/Principal Findings

We estimated the predation impact (‘kill rate’ and ‘predation rate’, i.e., number of prey and proportion of the prey population eaten, respectively) of Bonelli''s eagle Aquila fasciata on rabbit Oryctolagus cuniculus and red-legged partridge Alectoris rufa populations in two seasons (the eagle''s breeding and non-breeding periods, 100 days each) in SE Spain. The mean estimated kill rate by the seven eagle reproductive units in the study area was c. 304 rabbits and c. 262 partridges in the breeding season, and c. 237 rabbits and c. 121 partridges in the non-breeding period. This resulted in very low predation rates (range: 0.3–2.5%) for both prey and seasons.

Conclusions/Significance

The potential role of Bonelli''s eagles as a limiting factor for rabbits and partridges at the population scale was very poor. The conflict between game profitability and conservation interest of either prey or predators is apparently very localised, and eagles, quarry species and game interests seem compatible in most of the study area. Currently, both the persecution and negative perception of Bonelli''s eagle (the ‘partridge-eating eagle’ in Spanish) have a null theoretical basis in most of this area.     

Comparison of the Hunting Behavior of Four Piscine Predators Attacking Schooling Prey

Four piscine predator species were observed repeatedly attacking large (> 100,000) schools of flat-iron herring, Harengula thrissina. The predators could be categorized into two groups. Stalking predators (two species) were slow-moving, predominantly solitary hunters attacking from positions beneath the school. Attacks were directed at individual prey and the sequence of events was orient-approach-strike. Although the stalking species were seen most often and were responsible for the majority of the attacks, capture success was low. The remaining two species were fast-moving, pelagic hunters regularly occurring in groups of up to 8 individuals. These predators were extremely proficient at capturing prey, either by orienting on individuals (stragglers) or accelerating into the school and ramming their prey (impact attacks). Group size was positively associated with capture success, but not significantly so. Because stalking predators orient towards individual prey, they may suffer from the effect of confusion when attacking schooling prey. Use of the impact strategy, by comparison, may allow predators to overcome the confusion effect either by attacking prey already separated from the school, or by orienting towards aggregated prey rather than particular individuals.     

Assessing differential prey selection patterns between two sympatric large carnivores

Several conceptual models describing patterns of prey selection by predators have been proposed, but such models rarely have been tested empirically, particularly with terrestrial carnivores. We examined patterns of prey selection by sympatric wolves ( Canis lupus ) and cougars ( Puma concolor ) to determine i) if both predators selected disadvantaged prey disproportionately from the prey population, and ii) if the specific nature and intensity of prey selection differed according to disparity in hunting behavior between predator species. We documented prey characteristics and kill site attributes of predator kills during winters 1999–2001 in Idaho, and located 120 wolf-killed and 98 cougar-killed ungulates on our study site. Elk ( Cervus elephus ) were the primary prey for both predators, followed by mule deer ( Odocoileus hemionus ). Both predators preyed disproportionately on elk calves and old individuals; among mule deer, wolves appeared to select for fawns, whereas cougars killed primarily adults. Nutritional status of prey, as determined by percent femur marrow fat, was consistently poorer in wolf-killed prey. We found that wolf kills occurred in habitat that was more reflective of the entire study area than cougar kills, suggesting that the coursing hunting behavior of wolves likely operated on a larger spatial scale than did the ambush hunting strategy of cougars. We concluded that the disparity in prey selection and hunting habitat between predators probably was a function of predator-specific hunting behavior and capture success, where the longer prey chases and lower capture success of wolf packs mandated a stronger selection for disadvantaged prey. For cougars, prey selection seemed to be limited primarily by prey size, which could be a function of the solitary hunting behavior of this species and the risks associated with capturing prime-aged prey.