Sarah R Hoy

Steve J Petty

Alexandre Millon

D Philip Whitfield

Michael Marquiss

Martin Davison

Xavier Lambin
email: x.lambin@abdn.ac.uk

Age and sex-selective predation moderate the overall impact of predators

Keywords: Accipiter gentilis, mesopredator, northern goshawk, population dynamics, predatory interactions, recruitment, senescence, Strix aluco, superpredator, tawny owl

1. Currently, there is no general agreement about the extent to which predators impact prey population dynamics and it is often poorly predicted by predation rates and species abundances. This could, in part be caused by variation in the type of selective predation occurring. Notably, if predation is selective on categories of individuals that contribute little to future generations, it may moderate the impact of predation on prey population dynamics. However, despite its prevalence, selective predation has seldom been studied in this context. 2. Using recoveries of ringed tawny owls (Strix aluco) predated by 'superpredators', northern goshawks (Accipiter gentilis) as they colonized the area, we investigated the extent to which predation was sex and age-selective. Predation of juvenile owls was disproportionately high. Amongst adults, predation was strongly biased towards females and predation risk appeared to increase with age. This implies age-selective predation may shape the decline in survival with age, observed in tawny owls. 3. To determine whether selective predation can modulate the overall impact of predation, age-based population matrix models were used to simulate the impact of five different patterns of age-selective predation, including the pattern actually observed in the study site. The overall impact on owl population size varied by up to 50%, depending on the pattern of selective predation. The simulation of the observed pattern of predation had a relatively small impact on population size, close to the least harmful scenario, predation on juveniles only. 4. The actual changes in owl population size and structure observed during goshawk colonization were also analysed. Owl population size and immigration were unrelated to goshawk abundance. However, goshawk abundance appeared to interact with owl food availability to have a delayed effect on recruitment into the population. 5. This study provides strong evidence to suggest that predation of other predators is both age and sex-selective and that selective predation of individuals with a low reproductive value may mitigate the overall impact of predators on prey population dynamics. Consequently, our results highlight how accounting for the type of selective predation occurring is likely to improve future predictions of the overall impact of predation.

Introduction

Despite being a fundamental issue in ecology, the extent to which predators can impact prey population dynamics remains controversial, with some studies finding only a weak impact, whilst others reporting that an increase in predator abundance can cause up to a fourfold decrease in prey abundance (reviewed in [START_REF] Ritchie | Predator interactions, mesopredator release and biodiversity conservation[END_REF]. This highlights the complex nature of predator-prey interactions and suggests that the impact of predators on prey dynamics is moderated by factors other than predation rates and species abundances alone. The composition of many communities is currently changing, as species distributions shift in response to climate [START_REF] Walther | Ecological responses to recent climate change[END_REF] and with the restoration of ecosystems [START_REF] Maehr | Large Mammal Restoration: Ecological and Sociological Challenges in the 21st Century[END_REF][START_REF] Deinet | Wildlife comeback in Europe: The recovery of selected mammal and bird species[END_REF]. Consequently, improving predictions of the potential demographic impact of predation has become increasingly important for conservation and wildlife management purposes. Especially as many top predator species are of conservation interest [START_REF] Sergio | Intraguild predation in raptor assemblages: a review[END_REF][START_REF] Ritchie | Predator interactions, mesopredator release and biodiversity conservation[END_REF]. However, in order to improve predictions, the mechanisms involved in moderating the impact of predators on prey population growth rates (k) need to be identified.

In theory, variation in the degree of selectivity in predation occurring, defined here as the degree to which categories of prey are predated disproportionally to their relative abundance, is one mechanism which could cause a variety of demographic responses to predation. For example, in many long-lived species, the relative contribution made by different categories of individuals to population growth rates is likely to vary, as survival and reproductive output are both age and condition-dependent [START_REF] Jones | Senescence rates are determined by ranking on the fast-slow life-history continuum[END_REF]. Thus, if predation disproportionately affects categories of individuals with low survival and reproductive values, those that have a proportionally smaller effect on population dynamics, such as young, senescent and low-quality individuals, then the impact of predators on prey population dynamics may be different to that predicted from predation rates only. Furthermore, depending on the mating system of the prey species, sexselective predation has the potential to destabilize predator-prey dynamics [START_REF] Boukal | Does sex-selective predation stabilize or destabilize predator-prey dynamics[END_REF]. Therefore, in some circumstances, sex-selective predation may also have modulate the impact that predators have on prey populations. However, empirical evidence supporting this hypothesis remains scant [START_REF] Gervasi | Predicting the potential demographic impact of predators on their prey: a comparative analysis of two carnivoreungulate systems in Scandinavia[END_REF].

From the predator's point of view, optimal foraging theory predicts that predation should be biased towards categories of individuals that are easy to catch, either because they are encountered more frequently, are easy to detect, or because they are less able to escape predators [START_REF] Werner | Optimal foraging and size selection of prey by the bluegill sunfish (Lepomzs mochrochirus)[END_REF]. For example, juveniles are known to be predated at disproportionately high rates (e.g. [START_REF] Hammill | The role of predation in the ecology of the ringed seal in Barrow Strait, Northwest Territories, Canada[END_REF], which could have a knock-on effect on recruitment [START_REF] Koning | Long-term study on interactions between tawny owls Strix aluco, Jackdaws Corvus monedula and Northern Goshawks Accipiter gentilis[END_REF]. The ability to escape predators also varies amongst adults, with individuals in substandard condition being disproportionally predated (reviewed in [START_REF] Temple | Do predators always capture substandard individuals disproportionately from prey populations?[END_REF]. Furthermore, breeders are thought to be more vulnerable to predation than non-breeders (Magnhagen 1991 and references therein). As poor condition is associated with a higher predation risk, the physiological decline in condition after breeding could be one mechanism which explains why breeding often results in reduced future survival [START_REF] Williams | Natural selection, the cost of reproduction, and a refinement of lack's principle[END_REF]. In long-lived species, if the cost of previous breeding attempts and accompanying decline in condition accumulates with age, age-dependent vulnerability to predation in adults may arise conditionally on past reproductive decisions. Consequently, predation might increase the age-specific cost of reproduction and this mechanism of increasing predation risk with age could contribute to the decline in survival observed in most vertebrates [START_REF] Jones | Senescence rates are determined by ranking on the fast-slow life-history continuum[END_REF][START_REF] Nussey | Senescence in natural populations of animals: widespread evidence and its implications for bio-gerontology[END_REF]. However, few studies have examined whether predators select older individuals [START_REF] Spalding | Winter food of the cougar in southcentral British Columbia[END_REF][START_REF] Kunkel | Winter prey selection by wolves and cougars in and near Glacier National Park, Montana[END_REF].

'Superpredation' is a special type of predation where larger 'superpredators' kill smaller 'mesopredators'. In theory, mesopredators can defend themselves against superpredators using the teeth, claws or talons they use to kill prey. Consequently, the risk of injury associated with attacking other predators may be higher than when superpredators attack other prey. This could lead to different patterns of selective predation occurring. For example, sex-selective predation of sexually dimorphic species can be caused by size differences, as the larger sex may be a greater nutritional reward [START_REF] Hairston | The causes and consequences of sex-specific mortality in a freshwater copepod[END_REF]. However, in cases where both sexes are within the prey size range of the predator, if there is a higher risk of injury associated with attacking the larger mesopredator sex it might outweigh any nutritional benefit. Despite this, except for a higher vulnerability of juveniles, we know of no study that has quantified age and sex-selective patterns of superpredation. As mesopredators play an important role in the top-down control of ecosystems, the impact that superpredators can have on mesopredator dynamics can also have a 'cascade effect' on lower trophic levels [START_REF] Paine | Food webs: linkage, interaction strength, and community infrastructure[END_REF]). Thus, superpredation can affect the structure of whole communities and biodiversity of ecosystems [START_REF] Ripple | Wolves and the ecology of fear: can predation risk structure ecosystems[END_REF]reviewed in Ritchie & Johnson 2009). Despite this, interactions between superpredators and mesopredators are often ignored.

In spite of many studies suggesting that predation is selective on certain classes of individuals, the role of selective predation in moderating the overall impact of predators remains poorly known. Research linking selective predation to its subsequent effects on populations is needed to help determine whether such biases are responsible for variation in the impact of predators on population dynamics. Here, we take an empirical approach combined with a simulation exercise to determine whether predation of other predators (superpredation) is selective and examine the role of selective predation in moderating the overall impact of predators on prey populations. To do this, we take advantage of long-term longitudinal data collected on individuals of an established population of mesopredators, spanning the colonization and increase in abundance of a superpredator. Northern goshawks (Accipiter gentilis; hereafter goshawks) are known superpredators of several other avian predator species, such as tawny owls Strix aluco [START_REF] Mikkola | Owls killing and killed by other owls and raptors in Europe[END_REF][START_REF] Petty | The decline of Common Kestrels Falco tinnunculus in a forested area of northern England: the role of predation by Northern Goshawks Accipiter gentilis[END_REF]. Goshawks have been shown to selectively predate individuals of other prey species based on condition, sex and age [START_REF] Kenward | Hawks and doves: factors affecting success and selection in goshawk attacks on woodpigeons[END_REF][START_REF] Kenward | Goshawk winter ecology in Swedish pheasant habitats[END_REF][START_REF] Hoogland | Selective predation on Utah prairie dogs[END_REF]). However, whether goshawk predation on other predators is selective remains undetermined. Tawny owls are a sexually dimorphic long-lived mesopredator. Juvenile owls have a relatively low probability of survival and adult owl survival and reproduction declines with age [START_REF] Millon | Natal conditions alter age-specific reproduction but not survival or senescence in a long-lived bird of prey[END_REF]. Consequently, as both survival and reproduction are age-dependent, the relative contribution of each owl age class to k is likely to vary. Therefore, goshawk predation of tawny owls provides a suitable model for testing the hypothesis that if predation is disproportionally biased (selective) towards certain age classes, it will alter the overall impact of predation on prey population dynamics.

The objectives of this study are threefold. Firstly, using recoveries of ringed tawny owls predated by goshawks, we test whether superpredation is selective. More specifically, we tested the common belief that young inexperienced and elderly individuals are disproportionately taken by predators. We also predicted that predation would be biased towards males, because they are smaller than females and because males are more active they are generally thought to be more vulnerable to predation (Boukal, Berec & K rivan 2008 and references therein). Secondly, we aimed to determine whether selective predation modulates the overall impact of predation. We used age-specific population matrix models to simulate and compare the relative impact of several different patterns of selective predation on the tawny owl population, including the pattern observed in the first part of the study. Lastly, we explored whether the increase in goshawk abundance and concomitant predation had actually impacted tawny owl population characteristics, by testing for correlations between tawny owl population size, recruitment and immigration and goshawk abundance.

Materials and methods

study system

The study took place in Kielder Forest, northern England (55°13 0 N, 2°33 0 W); a man-made conifer forest. As the forest largely lacks natural tree cavities, the preferred nesting sites for tawny owls, owls readily started using the nest boxes which were provided in excess to the number of potential territories in a 176 km² central subsection of the forest [START_REF] Petty | Value of nest boxes for population studies of owls in coniferous forest in Britain[END_REF]. Each year, since 1979, occupied owl territories were identified and nearly all birds were uniquely marked with rings. Most breeding adults were caught each year (for details see Petty 1992a); females throughout the study period and males between 1988-1998 and 2008-2012. Adult owls were sexed by wing length, mass and the presence of a brood patch (Petty 1992a), and for 4 years, all chicks were sexed using DNA fingerprinting [START_REF] Appleby | Does variation of sex ratio enhance reproductive success of offspring in tawny owls (Strix aluco)[END_REF]. Un-ringed owls caught as adults were aged using primary feather moulting patterns from 1985 onwards (Petty 1992a,b). Therefore, the age of 98Á5% (N = 2216) of breeding owls in the population was known. Owl population size was measured as the total number of occupied territories, estimated for all except 6 years during the study period. Owl population dynamics may be influenced by food availability as the amount of vole prey available prior to the egg-laying stage (early spring) is positively associated with the number of owl pairs which attempt to breed and clutch size (Petty 1992a;[START_REF] Millon | Dampening prey cycles overrides the impact of climatic change on predator population dynamics: a long-term demographic study on owls[END_REF]. In Kielder, field voles (Microtus agrestis) are the main prey species for tawny owls in the study site [START_REF] Petty | Breeding of Tawny owls (Strix aluco) in relation to their food supply in an upland forest[END_REF][START_REF] Petty | Diet of tawny owls (Strix aluco) in relation to field vole (Microtus agrestis) abundance in a conifer forest in northern England[END_REF], and their densities hereafter referred to as owl food availability have been monitored bi-annually since 1985 (for methods see [START_REF] Lambin | Cyclic dynamics in field vole populations and generalist predation[END_REF].

Goshawks were absent in Kielder Forest until 1973 [START_REF] Petty | Goshawks Accipiter gentilis. The Atlas of Breeding Birds in Northumbria[END_REF]. Their subsequent spread has been continuously monitored over an area of 964 km², and approximately, 30 home ranges are currently occupied (Fig. 1). On average, goshawks (females: 1500 g, males: 850 g) are 2-3 times heavier than tawny owls (females: 520 g, males: 420 g) and are known to regularly kill them [START_REF] Mikkola | Owls killing and killed by other owls and raptors in Europe[END_REF][START_REF] Petty | The decline of Common Kestrels Falco tinnunculus in a forested area of northern England: the role of predation by Northern Goshawks Accipiter gentilis[END_REF]. Each year goshawk territories were searched for the remains of prey items, including tawny owl rings and when possible, nests were also searched for additional prey items. The goshawk monitoring area is more than five times larger than the tawny owl monitoring area. Goshawk pairs are known to have home ranges averaging 64 km² AE 16 (SE; [START_REF] Boal | Home range and residency status of Northern Goshawks breeding in Minnesota[END_REF] and territories are known to overlap [START_REF] Kenward | Predation on released pheasants (Phasianus colchicus) by goshawks (Accipiter gentilis) in central Sweden[END_REF]. Consequently, the entire tawny owl study site lay within the hunting range of goshawks. As goshawk home range size is highly variable [START_REF] Kenward | Goshawk hunting behaviour and range size as a function of food and habitat availability[END_REF] and is unknown in our study site, we used two proxies of predation risk for tawny owls (i) total goshawk abundance (the total number of goshawk territories known to be occupied); and (ii) local goshawk abundance (the number of occupied goshawk territories whose nests sites were within the estimated goshawk foraging distance of the owl monitoring area). Goshawk foraging distance was estimated as 5Á8 km, 85% of the maximal distance from the nest box last used by an owl to the goshawk nest where the owl ring was recovered.

age and sex-selective predation analyses

In order to determine whether goshawk predation was selective, the age and sex-selective pattern of ring recovered from goshawk nest sites were compared to those from other causes of mortality, Fig. 1. Amongst-year variation in the estimated number of territories occupied by tawny owls and northern goshawks, and spring (March-April) field vole densities in Kielder Forest, UK. such as starvation and collisions with vehicles, fences and buildings. As goshawk nest sites were deliberately targeted to recover owl rings, recoveries from other causes of mortality were only used to examine goshawk prey selectivity, not to infer the relative contribution of goshawk predation to owl mortality. The age at death was estimated for owls whose rings were recovered at goshawk nest sites. When carcasses were recovered with rings, the freshness of the carcass was used to estimate the month and year of death. The exact year at death could be determined for 92% (46) of the recoveries. Thus, a minimum age at death was estimated for 4% of the remaining recoveries using the date the owl was last captured alive, the year the goshawk nest was constructed and subsequently used and the years the goshawk territory was occupied. The remaining 4% of recoveries were from owls known to have died as adults, but the age at death could not be estimated. Such recoveries were excluded from the analysis specifically examining age-dependent predation of adults.

The first analysis tested whether goshawk predation was selective on juveniles (owls under 1 year old) or adults (owls over 1 year old). Fisher's exact test was used to determine whether the actual number of rings recovered for each age class (juveniles vs. adult) differed significantly from the number of rings expected to be recovered, if goshawk predation was random. The number of rings expected to be recovered was estimated by calculating the proportion of juveniles and adults in the population, using the age distribution of the owl population at equilibrium, predicted by the population matrix model (see Appendix S1, supporting information for details) and then multiplying it by the number of rings recovered from goshawk nest sites. The analysis was repeated on recoveries from other causes of mortality, and the results of the two analyses were compared. As the number of recoveries from adults was small, to determine whether predation on adult owls was age-selective, the proportion of all recoveries that were goshawk-related was analysed in relation to the owls' age at death using generalized linear models (GLMs) with a binomial error structure.

Sex-selective predation was determined using a binomial test to detect deviation of the sex ratio of predated recoveries from an expected even sex ratio. The same analysis was then repeated on recoveries from other causes of mortality and the results compared. Male and female owls were fitted with identically sized rings, so that a bias ring detection probability between sexes can be ruled out. To identify whether activities related to breeding could be responsible for any sex bias in predated recoveries, these analyses were repeated using owls that died as adults only.

simulated impact of selective predation

A post-breeding population matrix model with 17 age classes (juvenile and adults aged 1-16 years old) was parameterized using the survival parameters estimated by [START_REF] Millon | Pulsed resources affect the timing of first breeding and lifetime reproductive success of tawny owls[END_REF] and [START_REF] Millon | Natal conditions alter age-specific reproduction but not survival or senescence in a long-lived bird of prey[END_REF] (see Appendix S2, Supporting information for methods). This matrix model was used to estimate the age distribution of the population at equilibrium and simulate the effect of contrasted scenarios of selective goshawk predation on owl population size. Goshawk predation was simulated by removing a constant number of owls (N = 5) from the population each year. The initial population vector contained 200 adult females (over 1 year old) and the corresponding number of juveniles (i.e. fledglings) to match the age distribution at equilibrium. The age of the five individuals removed remained constant throughout the simulation and was set according to five contrasted patterns of selective predation: (i) the pattern of agespecific predation actually observed in Kielder Forest, determined by the ring recovery analysis; (ii) even where an equal number of individuals across all ages were removed; (iii) predation of juveniles only, where only juveniles (<1 year old) were removed; (iv) predation on young (prime-age) adults only, where an even distribution of young adult owls (aged 1-8 years old) were removed; and (v) predation of old adults only, where an even distribution of adults aged 9 years and older were removed. The cut-off for young (prime-aged) and old owls was set at 9 years of age because a previous analysis found some support for a threshold in female survival at 8 years of age after which survival was significantly lower than at age one, and female owls are also reproductively senescent at this age [START_REF] Millon | Natal conditions alter age-specific reproduction but not survival or senescence in a long-lived bird of prey[END_REF].

observed changes in owl population size and structure

As variation in food availability is also likely to impact tawny owl population dynamics, it was included as an explanatory variable when analysing the observed changes in owl population size and structure. To detect any impact that the selective goshawk predation actually occurring had on owl population size, variation in the number of territories occupied each year was analysed over time and in relation to the increase in goshawk abundance (measured as either total or local goshawk abundance) and changes in owl food availability. This was analysed over a 22-year period between 1985 and 2012 (excluding the 6 years where occupancy estimates were unavailable) using GLMs with a Poisson error structure.

The effect of goshawk predation on owl population size could potentially be masked by compensatory mechanisms such as increased recruitment or immigration. Therefore, variation in both were analysed in relation to goshawk abundance and food availability. Additionally, we tested for a temporal trend in both recruitment and immigration over a 28-year period between 1985 and 2012. To determine whether recruitment or immigration had changed, interannual variation in the proportion of newly recruited breeders in the population (those which had not recorded breeding previously) and the proportion of local recruits amongst all newly recruited breeders were analysed using GLMs with a Binomial error structure. If newly recruited owls into the population were ringed as chicks in Kielder Forest they were classified local recruits, or as immigrants if not. These analyses were restricted to females only as males were not caught throughout the entire study period. Descriptive statistics in the results section are the mean and standard deviation unless otherwise stated.

The additive and interactive effects of both owl food availability and goshawk abundance on owl population size, recruitment and immigration were tested. Explanatory variables were standardized so as to compare their effect sizes. We hypothesize that goshawk predation mainly occurs during the peak of the goshawk breeding season, which is after owl population size has been measured and recruitment of breeding owls has taken place. If this is the case, any effect of goshawk predation in that year may not become apparent until the following year. Consequently, the analyses looking at variation in owl population size and recruitment were repeated to test for the effect of a 1-year time lag. The probability of owls being recruited into the population in their first year is very small and the majority of owls start breeding between 2-3 years of age [START_REF] Millon | Pulsed resources affect the timing of first breeding and lifetime reproductive success of tawny owls[END_REF]. Consequently, any effect of goshawk predation and food availability on juvenile survival and thus the number of locally born owls available to be recruited is only likely to become evident after a 2-3 year lag. Therefore, the proportion of local recruits was analysed against explanatory variables after a 2-year and 3-year time lag. Model selection was based upon Akaike's information criterion corrected for small sample size (AICc, [START_REF] Burnham | Model Selection and Multimodel Inference[END_REF]. As total and local goshawk abundances were correlated (r = 0Á82, N = 28, P < 0Á001), their effects were examined in separate models. Neither measure of goshawk abundance was highly correlated with owl food availability (r = À0Á35, N = 28, P = 0Á07 for total goshawk abundance and r = À0Á17, N = 28, P = 0Á39 for local goshawk abundance). All analyses were carried out in R 3Á0Á3 (R Core Team 2014).

Results

age and sex-selective predation

During the study period, 2153 tawny owl chicks fledged. Overall, 16% of these fledglings were subsequently recaptured in the study area after reaching 1 year old and 3% were seen after 10 years old. The maximum age was 20 and 17 years for females and males respectively. A total of 108 ringed tawny owls were recovered, of which 50 (46%) were retrieved from goshawk nest sites. Of these, 34 (68%) were predated as juveniles. An exact age at death could be determined for 12 of the remaining 16 rings from adult owls recovered from goshawks nest sites and a minimum age at death for two others. The month of death could also be estimated for 12 of the adult recoveries. All of the owls were predated in June or July with the exception of one being predated in November. This peak in detected instances of adult predation coincides with when breeding tawny owls have large, fledged but dependant chicks whilst goshawks still have chicks in the nest. Collisions (mainly with vehicles) were the main cause of mortality for the 30 (52%) recoveries known to have died from other causes.

At equilibrium, the population matrix model estimated that juveniles made up 36% of the tawny owl population. Significantly, more juveniles were predated by goshawks than expected from their relative abundance in the population, 34 juvenile owl recoveries compared to the 18 expected (Fishers exact test: P < 0Á003, N = 50, odds ratio = 3Á7). In contrast, there was no discrepancy between the observed and expected number of juvenile recoveries (21 vs. 20) from other causes of mortality. The age distribution of adult owl recoveries from goshawk predation differed to that of other causes of mortality. The proportion of the owl population known to reach each age which were predated by goshawks increased with age, whereas recoveries from other causes of mortality did not (Fig. 2). The proportion of ringed owls recovered as goshawk kills amongst all causes of mortality, increased significantly with owl age (F 10 = 2Á48, P < 0Á01), with recoveries from birds estimated to have died over 9 years old three times more likely to have been predated by goshawks than dying from other causes of mortality.

Amongst adults, recoveries of predated owls differed significantly from an even sex ratio (Exact binomial test: P = 0Á04, N = 15). Recoveries were three times more likely to be from females than males (12 females and three males). Nine (75%) of adult females predated were recorded as breeding in the year they were predated. There was no excess of females amongst predated owls when an additional 12 rings from owls that died as juveniles (four females and eight males) were included in the analysis (P = 0Á44, N = 27, 16 females, 11 males). There was no departure from an even sex ratio of recoveries from other causes of mortality, irrespective of whether recoveries from juvenile were included (P = 0Á56, N = 26, 15 females and 11 males) or not (P = 0Á54, N = 24, 13 females and 11 males).

simulated impact of selective predation

The simulated impact of predation varied greatly between predation patterns from an 11% to 61% reduction in initial population size (percentages relate respectively to the simulation of predation on juveniles and predation of young adults only). The observed pattern of selective predation had a relatively small impact on population size, 12% more than the simulation of predation on juveniles alone, but less impacting than any of the other predation scenarios. Simulations of predation on young adults and even predation on all ages had the greatest impact, 50% and 28% more than the observed pattern of predation respectively. The simulated effect of predation on old adult owls (aged 9 years old and over) had a moderate impact on population size, 11% more than that of the observed pattern of predation but 18% less impacting than even predation on all ages (Fig. 3). For a full description of the population matrix model used and the estimated elasticity of tawny owl age-dependent demographic transitions see Appendices S2 and S3 (Supporting information) respectively.

observed changes in owl population size and structure

There was little interannual variation in the number of owl territories estimated to be occupied (56 AE 4Á07; Fig. 1). Variation in the number of occupied owl territories was not associated with either food availability or goshawk abundance and the null model performed best (see Table 1), irrespective of whether the effect of a time lag was included. There was no overall temporal trend in the proportion of newly recruited breeders in the owl population, suggesting recruitment has not changed overall. The null model performed best in terms of AICc when no time lag was considered. However, 50% of the variation in recruitment was explained by an interaction between local goshawk abundance and food availability when a 1year time lag was included (see Table 1). The proportion of newly recruited breeders in the population was relatively high when food availability and goshawk abundance were low in the preceding year. However, when goshawk abundance was high, the relationship between food availability and recruitment was weaker (Fig. 4). The proportion of local recruits in the population decreased significantly (F 26 = À3Á15, P < 0Á01) by 38% from 0Á48 AE 0Á25 in the first 5 years of the study period to an average of 0Á30 AE 0Á19 in the last 5 years. There was a positive correlation between the proportion of new recruits that were born locally and food availability, which explained 20% and 15% of the variation in immigration when a 2 and 3-year time lag was considered respectively (Fig. 5).

Discussion

Predation of tawny owls was sex and age-selective, with juveniles more vulnerable to goshawk predation than adults. Predation of adults was also selective towards females and older individuals, especially those over 8 years old. A result consistent with predation contributing to the senescence in survival observed in tawny owls. These results contrast with those from other causes of mortality, which showed no indication of any age or sexselection and suggest that goshawks selectively predate individuals of low reproductive value (juveniles and older individuals) that contribute relatively little to k. The simulation experiment supported the hypothesis that age-selective predation can moderate the overall impact of predation, as there was up to a 50% difference in overall impact between the contrasted patterns of age-selective predation. The simulated impact of the observed pattern of selective predation on owl population size was relatively small, particularly when compared to the simulation of no age-selective predation or predation of young adults. The number of occupied owl territories (owl population size) remained constant throughout the study period in Kielder Forest and was seemingly unaffected by changes in goshawk abundance. Overall, these results match our hypothesis that if predators primarily target individuals which contribute less to k the actual impact of goshawk predation on the tawny owl population should be relatively small.

age and sex-selective predation

As expected, predation of juveniles was disproportionately high; a result concordant with other studies investigating superpredation in birds of prey [START_REF] Petty | The decline of Common Kestrels Falco tinnunculus in a forested area of northern England: the role of predation by Northern Goshawks Accipiter gentilis[END_REF][START_REF] Sunde | Predators control post-fledging mortality in tawny owls, Strix aluco[END_REF][START_REF] Koning | Long-term study on interactions between tawny owls Strix aluco, Jackdaws Corvus monedula and Northern Goshawks Accipiter gentilis[END_REF]. Fledgling tawny owls may be more vulnerable to goshawk predation than adults as they are unable to fly properly when they first leave the nest [START_REF] Petty | A radio tracking study of post-fledging mortality and movements of Tawny Owls in Argyll[END_REF][START_REF] Sunde | Reversed sexual dimorphism in tawny owls, Strix aluco, correlates with duty division in breeding effort[END_REF]. Additionally, they produce begging calls during the day, making them more conspicuous to diurnal predators, such as goshawks [START_REF] Petty | The decline of Common Kestrels Falco tinnunculus in a forested area of northern England: the role of predation by Northern Goshawks Accipiter gentilis[END_REF]. Therefore, fledglings may be easier to locate than adult owls which generally only call at night [START_REF] Mikkola | Owls of Europe[END_REF].

Predation of adult owls was strongly female biased, despite male-biased predation being 2Á3 times more common across a range of taxonomic groups (reviewed in [START_REF] Boukal | Does sex-selective predation stabilize or destabilize predator-prey dynamics[END_REF]. This result contrasts with Fig. 3. The predicted impact, in terms of the percentage reduction in initial population size for five different patterns of ageselective predation on a theoretical tawny owl population simulation over 20 years. Observed relates to the simulation of the actual pattern of selective predation observed in the study site. Even is the simulated effect of equal predation on all ages; juvenile, the simulation of predation only on individuals less than 1 year old; young, the simulated effect of even predation on adult owls aged 1-8 years. Old represents even predation on owls aged 9 years and over.

the lack of any such sex-selection in owl recoveries from other causes of mortality and contradicts our prediction that predation of owls would be male biased, as males are more active doing the majority of hunting during the breeding season. Sex-selective predation can be caused by differences in parental roles that make one sex more vulnerable to predation [START_REF] G€ Otmark | Natural selection and sexual dimorphism: sex-biased sparrowhawk predation favours crypsis in female chaffinches[END_REF][START_REF] Svensson | Fish predation on Eudiaptomus gracilis in relation to clutch size, body size, and sex: a field experiment[END_REF]. For example, increased vulnerability of females during incubation and brooding was cited as the main cause of sex-selection in game birds predated by goshawks [START_REF] Kenward | Predation on released pheasants (Phasianus colchicus) by goshawks (Accipiter gentilis) in central Sweden[END_REF][START_REF] Wid En | Goshawk predation during winter, spring and summer in a boreal forest area of central Sweden[END_REF]. However, as tawny owls are cavity-nesters, females are unlikely to be vulnerable (in terms of exposure) to avian predation during the majority of this period. However, after fledging, juvenile begging calls may make female owls easier to detect than males as they remain closer to their offspring once the chicks have left the nest box [START_REF] Sunde | Reversed sexual dimorphism in tawny owls, Strix aluco, correlates with duty division in breeding effort[END_REF]. Additionally, females may become vulnerable to predation when protecting their brood [START_REF] Mikkola | Owls of Europe[END_REF]). Such differences in parental roles are thought to cause sex-selective predation in other species. For example, male Malagasy giant rats, Hypogeomys antimena, have a higher risk of being predated as they remain closer to and invest more in the welfare of their offspring than females [START_REF] Sommer | Sex specific predation rates on a monogamous rat (Hypogeomys antimena, Nesomyinae) by top predators in the tropical dry forest of Madagascar[END_REF].

The high proportion of adult owls recorded as breeding in the year they were predated supports the hypothesis that reproduction increases vulnerability to predation. Given most recorded instances of adult owls being predated were in June and July, after owl chicks have fledged, it suggests that vulnerability to predation is related to reproductive costs incurred before the fledgling stage or changes in behaviour at the fledging stage. In birds, the cost of previous reproduction can manifest itself as fewer feathers being replaced by breeding birds (Pi-eti€ ainen, Saurola & Kolunen 1984;[START_REF] Petty | Moult in tawny owls Strix aluco in relation to food supply and reproductive success[END_REF] or poorer quality plumage produced by breeders [START_REF] Dawson | Rate of moult affects feather quality: a mechanism linking current reproductive effort to future survival[END_REF]. Female tawny owls moult fewer primary feathers per year than males after breeding and moult c. 30% fewer primaries than non-breeding owls [START_REF] Petty | Moult in tawny owls Strix aluco in relation to food supply and reproductive success[END_REF]. This suggests the cost of reproduction is higher for females and, as a consequence, female flight ability may be lower than males after breeding. Furthermore, female flight feather condition may degrade more than males during Table 1. Results of analysis and model selection examining the effect of food availability (field vole densities in spring) and goshawk abundance on (a) tawny owl population size (number of occupied territories) and recruitment (the proportion of female breeders newly recruited) each year, modelled against explanatory variables from the same year and with 1 year delayed effect (1-year lag effect). (b) Immigration (the proportion of newly recruited breeders into the tawny owl population which were born locally) with a 2 and 3-year delayed effect. As models with each measure of goshawk abundance performed very similarly, only one measure for each analysis is presented in the the breeding season, due to abrasion against the sides of the nest-cavity and spending less time preening and exercising flight muscles whilst incubating eggs and brooding young chicks. All of which is likely to result in females having reduced feather condition after breeding. Given poor-quality plumage can result in inferior flying performance [START_REF] Swaddle | Plumage condition affects fight performance in common starlings: implications for developmental homeostasis, abrasion and molt[END_REF], we propose that, after breeding, females have a reduced ability to escape predators. The above conjectures could explain why no sex-selectivity was observed when recoveries from juveniles were also included. Predation of adult owls also appeared age-dependent, as the proportion of all ring recoveries that were goshawk-related increased with age. For species, like tawny owls which do not do a full moult annually, the cost of reproduction in terms of reduced feather quality (fewer feathers replaced by breeders) is likely to accumulate with age following successive breeding attempts. This could potentially be the mechanism causing the observed increase in vulnerability to predation with age and thus contribute to the pattern of senescence in survival observed in tawny owls. After 8 years of age, the proportion of all recoveries that were predated was higher than that of other causes of mortality. This implies that after this age, the risk of being predated increases for female owls. This coincides with a decline in female owl survival, as survival of 9-year-old females was significantly lower than at age one [START_REF] Millon | Natal conditions alter age-specific reproduction but not survival or senescence in a long-lived bird of prey[END_REF]. Consequently, these results provide some support for our hypothesis that agedependent predation risk contributes to the decline in survival observed in long-lived species.

Overall, our results support the hypothesis that the accumulation of reproductive costs over a lifetime and subsequent decline in condition leads to increased vulnerability to predation with age. Interestingly, it implies that the cost of reproduction for this long-lived species is fully evident in the presence of a predator, and conversely, that the trade-off between reproduction and moulting may not be visible in environments lacking top predators. Thus, we posit that the observed age and sex-selective predation were caused by a combination of (i) juveniles and females being easier to detect; and (ii) the ability to escape predator attacks being age and sex-dependent due to the accumulation of reproductive costs, with age. simulated and observed impact of selective predation on owl population size and structure Despite goshawks predating owls relatively frequently in our study site, tawny owl population size seemed unaffected by the increasing goshawk population. Our simulations of contrasted selective predation patterns indicates that the observed pattern of predation by goshawks is very close the least harmful scenario, having a relatively small impact on total population size. This combined with the observation that goshawks appeared to selectively predate individuals with low reproductive values (juveniles and older females) matches the prediction that, if predation is restricted to categories of individuals with low reproductive values, the overall impact of predators on prey population dynamics will be lower than that predicted by predation rates alone. A conclusion further supported by the lack of a relationship between goshawk abundance and owl population size.

There was no evidence to suggest that an increase in recruitment into the population could be masking the effect of goshawk predation on the population, as there was no overall change in the proportion of breeders newly recruited into the population during the study period. However, goshawk abundance did appear to interact with owl food availability to have a combined effect on recruitment in the following year. We posit that when food is highly abundant and predation risk is low, more breeders survive to the following year, thus fewer territories become available for new breeders resulting in a low proportion of new recruits in the breeding population. However, when goshawk abundance is high, presumably so is the risk of owls being predated, which may reduce any positive effect of high food availability on owl survival. This could explain why the proportion of new recruits in the population was relatively low when owl food availability was high and goshawk abundance was low in the preceding year and why the effect of food availability and recruitment was weaker when goshawk abundance was high. Although owl population size and overall recruitment appeared to remain constant, there was a significant decrease in local birds being recruited into the population; this implies there is a shortage of local recruits. The positive correlation between owl food availability and the proportion of local recruits after a 2-and 3-year lag is consistent with the findings of [START_REF] Millon | Pulsed resources affect the timing of first breeding and lifetime reproductive success of tawny owls[END_REF]. This suggests that the decline is most likely caused by a reduction in owl productivity and potentially juvenile survival due to declining food availability in spring and changing climate [START_REF] Millon | Dampening prey cycles overrides the impact of climatic change on predator population dynamics: a long-term demographic study on owls[END_REF]. Although predation of juveniles may also contribute to a shortage of local recruits, our analyses suggest it does not exacerbate the effect of declining food availability on local owl recruitment significantly.

Overall, our results imply that selective predation can alter the impact of predators on prey populations and highlight the importance of examining the type and extent of selective predation occurring when assessing and predicting the potential impact of predators. We conclude that superpredation, goshawk predation of adult owls is both age and sex-selective; however, the pattern of selective goshawk predation occurring in our study system is insufficient to affect tawny owl population size. Thus, selective predation combined with other compensatory mechanisms such as immigration may play an important role in modulating and buffering the overall impact of predators.

Fig. 2 .

 2 Fig. 2. Expected age distribution at equilibrium of adult tawny owls aged 1-14 years predicted by a population matrix model (white bars).The percentage of tawny owls known to reach each age that were predated by northern goshawks or died from other causes are shown by black and grey respectively.

Fig. 5 .

 5 Fig. 5. Variation in the proportion of newly recruited breeding female tawny owls which were born locally each year according to mean vole density in spring the previous (a) 2 years (b) 3 years. Point size is proportional to the number of new recruits in the current year (range: 1-22).

Fig. 4 .

 4 Fig. 4. Annual proportion of breeding female tawny owls which were newly recruited according to mean vole density in spring the previous year. Solid black points represent proportions when local goshawk abundance was relatively high (10 or more occupied territories) in the previous year. White points represent proportions when goshawk abundance was low (<10 occupied territories) in the preceding year. Point size is proportional to the number of pairs breeding in the current year (range: 4-61).

  table. For each analysis, the model with the lowest AICc is in bold

				Same year						1-year lag effect
			Explanatory
	a) Response variable		variable	Estimate	S.E	d.f. DAICc		Estimate S.E	d.f. DAICc
	Owl population size	1. Null	-		-	21	0Á00	1. -	-	20	0Á00
	(Number of occupied	2. Food availability		0Á041	0Á028 20	0Á25	2.	0Á003	0Á029 19	2Á44
	owl territories)	3. Total goshawk		0Á022	0Á029 20	1Á83	3. À0Á010	0Á029 19	2Á35
		4. Food availability +		0Á054	0Á029 19	1Á26	4.	0Á001	0Á030 18	5Á09
			Total goshawk		0Á039	0Á030					À0Á009	0Á030
		5. Food availability		0Á053	0Á030 18	4Á27	5.	0Á001	0Á030 17	8Á18
			Total goshawk		0Á039	0Á031					À0Á010	0Á031
			Interaction	À0Á003	0Á029					À0Á002	0Á031
	Recruitment (Proportion	1. Null	-		-	27	0Á00	1. -	-	26	14Á89
	of breeding females	2. Food availability	À0Á049	0Á071 26	1Á84	2. À0Á308	0Á094 25	5Á64
	newly recruited)	3. Local goshawk	À0Á008	0Á083		2Á32	3. À0Á148	0Á085 25	14Á14
		4. Food availability + À0Á055	0Á074 25	4Á27	4. À0Á311	0Á094 24	4Á75
			Local goshawk	À0Á026	0Á086					À0Á153	0Á083
		5. Food availability	À0Á049	0Á076 24	6Á82	5. À0Á279	0Á100 23	0Á00
			Local goshawk	À0Á020	0Á087					0Á026	0Á105
			Interaction		0Á044	0Á099					0Á389	0Á144
					2-year lag effect					3-year lag effect
	b) Response variable		Explanatory variable	Estimate	S.E	d.f.	DAICc		Estimate	S.E	d.f.	DAICc
	Immigration (Proportion	1.	Null		-	-	25		5Á50	1.	-	-	24	3Á55
	of newly recruited	2.	Food availability		0Á410	0Á151	24		0Á00	2.	0Á347	0Á146	23	0Á00
	females born locally)	3.	Total goshawk		À0Á113	0Á140	24		7Á19	3.	À0Á187	0Á156	23	4Á44
		4.	Food availability +		0Á401	0Á153	23		2Á46	4.	0Á329	0Á158	22	2Á51
			Total goshawk		À0Á047	0Á142					À0Á049	0Á170
		5.	Food availability		0Á458	0Á162	22		3Á73	5.	0Á343	0Á161	21	5Á19
			Total goshawk		À0Á042	0Á142					À0Á096	0Á202
			Interaction		0Á253	0Á203					0Á068	0Á157

© 2014 The Authors. Journal of Animal Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society., Journal of Animal Ecology, 84, 692-701

Acknowledgements

Thanks to J. Reid, S. Redpath, A. Beckerman and an anonymous reviewer for their helpful comments on a previous version of the manuscript. This work was partly funded by a Natural Environment Research Council studentship NE/J500148/1 to SH and a grant NE/F021402/1 to XL and by Natural Research Limited. Forest Research funded all the fieldwork on goshawks, tawny owls and field voles during 1973-1996. We thank B. Little, P. Hotchin, D. Anderson and all field assistants for their help with data collection and Forest Enterprise, T. Dearnley and N. Geddes for allowing and facilitating work in Kielder Forest. In addition, we are grateful to English Nature and the BTO for kindly issuing licences annually visit goshawk nest sites.

Data accessibility

All data associated with the study which have not already been given in the text are available from the Dryad Digital Repository: http://doi.org/ 10.5061/dryad.h1289 [START_REF] Hoy | Data from: Age and sex-selective predation as moderators of the overall impact of predation[END_REF].

Supporting Information

Additional Supporting Information may be found in the online version of this article.


A Gérard

H Jourdan

A Millon

E Vidal

Anti-predator behaviour in a procellariid seabird: Wedge-tailed shearwaters do not respond to the odour of introduced ship rats

Keywords: avoidance behaviour, introduced rodent, invasive species, Procellariiformes, Y-maze experiment

Seabirds are particularly vulnerable to introduced alien mammalian predators, especially invasive rats, which are the main contributors to seabird extinction and endangerment in many places worldwide. However, this appears context-dependent because, paradoxically, cases of apparent long-term coexistence between rats and some species of seabird have been reported for centuries, in various locations. Among seabirds, procellariiforms are known to have developed a range of olfactory-driven behaviours, such as partner recognition and homing. Olfaction could be an effective means of recognizing and thereafter avoiding invasive predators. However, the role of olfaction in predation risk assessment has not yet been examined in any procellariiform. Here, we investigated, through a Y-maze experiment, whether the wedge-tailed shearwater (Puffinus pacificus) avoided the odour of one of the most damaging alien predators on islands, the ship rat (Rattus rattus). The experiment was conducted in different ecological contexts on three neighbouring islets off New Caledonia having different communities of invasive rats. Contrary to our expectations, the wedge-tailed shearwater either did not detect or did not avoid the odour of the ship rat, despite about 175 years of coexistence between rats and shearwaters in New Caledonia. These findings highlight the need for further investigations (across species, across sites) into the factors underpinning the paradox between high vulnerability and the surprising long-term coexistence between procellariid seabirds and alien invasive rats.

INTRODUCTION

Introduced mammals, especially predators, are known to have severely impacted island birds worldwide, including seabird species (e.g. [START_REF] Owens | Ecological basis of extinction risk in birds: habitat loss versus human persecution and introduced predators[END_REF][START_REF] Courchamp | Mammal invaders on islands: impact, control and control impact[END_REF][START_REF] Hervias | Studying the effects of multiple invasive mammals on Cory's shearwater nest survival[END_REF][START_REF] Spatz | The biogeography of globally threatened seabirds and island conservation opportunities[END_REF]. Rats (Rattus sp.) in particular have colonized about 90% of the world's islands [START_REF] Atkinson | The spread of commensal species of Rattus to oceanic islands and their effects on island avifaunas[END_REF][START_REF] Towns | Have the harmful effects of introduced rats on islands been exaggerated?[END_REF] and are among the main contributors to seabird extinction and endangerment documented worldwide, particularly for small-to medium-sized procellariid seabirds such as petrels and shearwaters [START_REF] Jones | Severity of the effects of invasive rats on seabirds: a global review[END_REF][START_REF] Shiels | Biology and impacts of Pacific Island invasive species. 11. Rattus rattus, the black rat (Rodentia: Muridae)[END_REF]. The vulnerability of petrels and shearwaters to invasive rats is enhanced by their ground-or burrow-nesting habits, which make the eggs, chicks and incubating adults easy prey (e.g. [START_REF] Warham | The Behaviour, Population Biology and Physiology of the Petrels[END_REF][START_REF] Jones | Severity of the effects of invasive rats on seabirds: a global review[END_REF]. Like many species having evolved in the absence of predators on isolated islands, petrels and shearwaters gen-erally exhibit no or ineffective anti-predator behaviour when facing alien predators [START_REF] Warham | The Behaviour, Population Biology and Physiology of the Petrels[END_REF][START_REF] Carthey | Naïveté in novel ecological interactions: lessons from theory and experimental evidence[END_REF].

Nevertheless, several cases of apparent long-term coexistence between rats and seabirds have been reported on many islands around the world [START_REF] Catry | Can thin-billed prions Pachyptila belcheri breed successfully on an island with introduced rats, mice and cats? The case of New Island, Falkland Islands[END_REF][START_REF] Quillfeldt | Introduced mammals coexist with seabirds at New Island, Falklands: abundance, habitat preferences and stable isotope analysis of diet[END_REF][START_REF] Ruffino | Invasive rats and seabirds after 2,000 years of an unwanted coexistence on Mediterranean islands[END_REF]). These paradoxical situations suggest that the impact of rats on seabirds could be context dependent, that is, may vary according to the period when seabirds are available as prey (returning to the land) and to the availability of alternative food resources during the year [START_REF] Rayner | Spatial heterogeneity of mesopredator release within an oceanic island system[END_REF]. Alternatively, some seabirds may sometimes manage to chase away rats through aggression or nest defence behaviour [START_REF] Warham | The Behaviour, Population Biology and Physiology of the Petrels[END_REF]. Procellariid seabirds may also have locally developed indirect, cryptic anti-predator behaviours so as to reduce the impact of rats (e.g. [START_REF] Ruffino | Invasive rats and seabirds after 2,000 years of an unwanted coexistence on Mediterranean islands[END_REF][START_REF] Bourgeois | Dramatic increase in the Zembretta Yelkouan shearwater breeding population following ship rat eradication spurs interest in managing a 1500-year old invasion[END_REF]. Interestingly, the extent and the rapidity of some seabird population recovery after rat eradication [START_REF] Bourgeois | Dramatic increase in the Zembretta Yelkouan shearwater breeding population following ship rat eradication spurs interest in managing a 1500-year old invasion[END_REF] suggest that rats had previously prevented birds from breeding, and points to an as yet unidentified behavioural process enabling shearwaters to detect and avoid rat-infested islands, and to rapidly (re)colonize islands when rats are removed.

The use of olfaction to assess predation risk is common across species of vertebrates [START_REF] Kats | The scent of death: chemosensory assessment of predation risk by prey animals[END_REF], and it has recently been suggested that olfaction and chemical communication in birds may be more important than previously thought [START_REF] Steiger | Avian olfactory receptor gene repertoires: evidence for a well-developed sense of smell in birds? P. Roy[END_REF][START_REF] Bonadonna | Besides colours and songs, odour is the new black of avian communication[END_REF]. Procellariid seabirds in particular use chemical communication and their sense of smell for many purposes, including identification of foraging areas [START_REF] Nevitt | Olfactory foraging by Antarctic procellariiform seabirds: life at high Reynolds numbers[END_REF][START_REF] Nevitt | Seeing the world through the nose of a bird: new developments in the sensory ecology of procellariiform seabirds[END_REF], homing and nest recognition (Bonadonna et al. 2003a,b;Bonadonna et al. 2004), or partner recognition [START_REF] Bonadonna | Partner-specific odor recognition in an Antarctic seabird[END_REF]). The ability to use chemical cues to ascertain predator presence and assess predation risk could be crucial for species nesting in cavities, that is, habitats where visual detection of predators is not easy [START_REF] Amo | Predator odour recognition and avoidance in a songbird[END_REF]). This has recently been tested for hole-nesting songbirds (e.g. [START_REF] Godard | Eastern bluebirds Sialia sialis do not avoid nest boxes with chemical cues from two common nest predators[END_REF][START_REF] Amo | Predator odour recognition and avoidance in a songbird[END_REF][START_REF] Roth | Can foraging birds assess predation risk by scent?[END_REF][START_REF] Amo | Smelling out predators is innate in birds[END_REF]) with positive and negative results. In fact, three of these studies showed that songbird species detected predator odours and showed anti-predator behaviour to cope with the risk of predation [START_REF] Amo | Predator odour recognition and avoidance in a songbird[END_REF][START_REF] Amo | Smelling out predators is innate in birds[END_REF][START_REF] Roth | Can foraging birds assess predation risk by scent?[END_REF], whereas the last one showed that the presence of chemical cues of nest predators does not ultimately influence selection of nest site by eastern bluebird (Sialia sialis) [START_REF] Godard | Eastern bluebirds Sialia sialis do not avoid nest boxes with chemical cues from two common nest predators[END_REF]). However, to the best of our knowledge, the use of chemical cues to detect predators has never been investigated in procellariid seabirds.

To fill this gap, we experimentally tested whether the wedge-tailed shearwater (Puffinus pacificus) could detect and respond to the odour of the ship rat. Experiments were conducted in the southern lagoon of New Caledonia, which hosts what is probably one of the world's largest colonies of P. pacificus [START_REF] Benoit | Seabirds of the southern lagoon of New Caledonia; distribution, abundance and threats[END_REF]. The ship rat can dramatically reduce the breeding success of P. pacificus, as documented on two Hawaiian islands, where the breeding success of birds sharply increased following rat eradication [START_REF] Smith | Recovery of native species following rat eradication on Mokoli'i Island, O'ahu, Hawai'i[END_REF][START_REF] Vanderwerf | Response of wedge-tailed shearwaters (Puffinus pacificus) to eradication of black rats (Rattus rattus) from Moku'auia Island after reinvasion[END_REF]).

METHODS

Study system

This study was conducted on breeding colonies of P. pacificus on three islets off Isle of Pines (22°37′S, 167°29′E), New Caledonia (South Pacific Ocean) in 2012. These islets, hereafter called islets A, B and C, are protected areas with restricted access for non-scientific activities. Their surface areas are respectively 33.6, 10.0 and 19.3 ha. The islets are formed of uplifted coral blocks, with typical coastal forest on limestone substrate and sandy beaches housing shearwater colonies. Tests were performed between 11 November and 6 December, that is, the period when P. pacificus returns to the colonies searching for mates, refurbishing existing burrows or digging new ones. We hypothesized that birds are particularly sensitive to predators' odours at this crucial stage of the breeding cycle. Puffinus pacificus weigh an average of 389 ± 31 g (N = 113, Brooke 2004), spend most of their lives at sea, with intermittent returns to the islands during the breeding period (October to April).

The ship rat was introduced into New Caledonia by European settlers around 1850, whereas the smaller Pacific rat was introduced into New Caledonia much earlier, about 3000 years ago by Melanesian colonizers [START_REF] Pascal | Les peuplements néo-calédoniens de vertébrés: invasions, disparitions[END_REF]). Our study islets A and B hosted the ship rat but were free of the Pacific rat, whereas islet C was free of the ship rat but hosted the Pacific rat. The presence/absence of the two rat species was confirmed by a total of 700 trap-nights conducted on the islets.

Olfactory experiment setting

The experiment consisted of a standard binary choice test using a portable Y-maze involving the choice between two exit arms [START_REF] Grubb | Olfactory navigation to the nesting burrow in Leach's petrel (Oceanodroma leucorrhoa)[END_REF]Bonadonna et al. 2003a;[START_REF] Bonadonna | Partner-specific odor recognition in an Antarctic seabird[END_REF]). The Y-maze was built from a single opaque Polyvinyl chloride (PVC) tube (16 cm of diameter) divided into three sections (Fig. 1), to avoid any difference between arms that might influence the bird's choice. The start arm had a temporary bird-holding compartment at its entrance. The two exit arms each contained a paper towel either scented with ship rat odour (obtained from seven wildtrapped ship rats and by placing paper towels on the floor of cages containing rats to collect urine and faeces) or unscented (soaked with distilled water). To avoid human scent contamination, the paper towels were prepared with latex gloves and handled with metal pliers (one pair of pliers to handle the unscented paper towels and another pair for the paper towels carrying the ship rat odour). For each test, new gloves were used, and the pliers were cleaned with 95% ethanol.The paper towels were placed on the lower surface of the tube, half way along each exit arm.The bird therefore had to walk over one of the paper towels before leaving the maze. New paper towels, either scented or unscented, were used for each test. The entire maze was cleaned with 95% ethanol after each test to remove any odour (i.e. rat and shearwater).

The same arm contained the ship rat odour in each test, to avoid potential bias due to any presence of residual rat odour (after cleaning) in the arm considered as the control arm. This involved disassembling and interchanging the arms between bird trials so that the odour was sequentially located on the left and on the right, allowing time (about 10 min) for the ethanol to evaporate before the next test.

Birds were caught early at night on the ground, when they landed at the colony. There is unfortunately no ringing programme on P. pacificus in the study area, so age or reproductive status of individuals (prospecting or breeding bird) could not be determined. Each bird was then placed individually in a new cotton bag (i.e. with no residual odour of other birds), transported to the maze and placed in the holding compartment for a 5-min acclimation period (Bonadonna et al. 2003a,b;[START_REF] Bonadonna | Partner-specific odor recognition in an Antarctic seabird[END_REF]Bonadonna et al. 2004). The maze was placed outside the colony (approximately 50-100 m) to reduce possible interference from birds flying and calling in the vicinity. Both exit arms were oriented toward the edge of the forest habitat, that is, toward a similar dark and uniform area, to avoid a possible visual effect on exit choice.The entrance of the maze faced the sea to avoid (i) the wind entering the two exit arms and potentially intensifying odour diffusion disproportionately in one arm, and (ii) odours from outside entering the two exit arms.

After the trap door was raised, we recorded the bird's choice between scented/control arms to escape the maze. No individual visited the two arms before exiting. Total handling time (from capture to exit) did not exceed 25 min: 10 min between capture and acclimation period, 5 min of acclimation, and 5-10 min to exit the maze. Only a few birds left the maze without prompting. If the bird did not leave the holding compartment after 5 min, we gently knocked on the door to rouse it from its quiescent state and prompt it to move. This procedure has previously been found not to affect birds' choice between two chambers [START_REF] Amo | Male quality and conspecific scent preferences in the house finch, Carpodacus mexicanus[END_REF]. In our experiments, no individual left the maze immediately following our 'knocking'; all the birds took time (5-10 min) choosing between the scented and unscented arms before exiting. This indicates that the birds' choice of exit was not affected by prompting, and a response was recorded for all birds tested. As the birds left the experimental device, they were recaught and then released at their initial capture location. Each bird was marked with a dash on the palm of its foot by a permanent marker, so as to avoid birds being tested several times.

Overall, a total of 100 different birds were tested (45 on islet A, 15 on islet B and 40 on islet C). The binary response variable (0: scented arm; 1: unscented arm) was modelled according to the ecological conditions on the islets (a threelevel factor for islets A, B, C), using a generalized linear model with a binomial distribution of error and a logit link (implemented in R 2.15.0; R Development Core Team 2012). We assessed whether the bird avoidance rating (proportion of birds choosing the unscented/control arm) differed from a random choice (intercept fixed at 50%). A power analysis, based on a binomial process with a threshold set at 80%, indicated an avoidance rating of 0.65, 0.70 and 0.72 respectively for a sample size of 100, 60 and 40.

RESULTS

For each islet, the number of choices of right arm versus left arm showed no lateral preference (P > 0.46).

Selection by P. pacificus of rat-scented/unscented arms to exit the plastic Y-maze did not differ from random (Fig. 2;Table 1). On islet A, 23 out of 45 birds left through the unscented arm, 7 out of 15 on islet B, and 23 out of 40 on islet C. Pooling the islets with ship rats (A and B) versus the islet without ship rats (islet C) gave a similar result (Table 1). The avoidance rate was therefore very close to 50% whatever the islet (51%, 47% and 57% respectively for islets A, B and C), and irrespective of the presence or absence of the ship rat (50% for islets A and B with ship rats present and 57% for islet C with no ship rats).

DISCUSSION

Our results show that the P. pacificus either did not detect the odour of the ship rat or, if they detected it, did not avoid it. This result holds true irrespective of whether ship rats were present on the islet housing the shearwater colony, and is rather surprising given the high vulnerability of Puffinus spp. to rats, particularly the ship rat [START_REF] Lock | Eradication of brown rats Rattus norvegicus and black rats Rattus rattus to restore breeding seabird populations on Lundy Island, Devon, England[END_REF][START_REF] Smith | Recovery of native species following rat eradication on Mokoli'i Island, O'ahu, Hawai'i[END_REF][START_REF] Jones | Severity of the effects of invasive rats on seabirds: a global review[END_REF][START_REF] Rando | Evidence for a second western Palaearctic seabird extinction during the last millennium: the lava shearwater Puffinus olsoni[END_REF][START_REF] Spatz | The biogeography of globally threatened seabirds and island conservation opportunities[END_REF]. The power analysis indicated that our experimental sample size was adequate to detect a biologically relevant difference.

Even though the possibility that stress following capture impaired the birds' ability to respond to odour cannot entirely be ruled out, great care was taken to avoid this bias. In particular, the experiment was designed to minimize stress for individuals (e.g. short handling time, acclimation period before tests). Moreover, similar experiments testing the odours of partners [START_REF] Bonadonna | Partner-specific odor recognition in an Antarctic seabird[END_REF] or nests (Bonadonna et al. 2003a,b;Bonadonna et al. 2004) have been successfully conducted on other procellariid seabirds (Antarctic prion Pachyptila desolata, common diving petrel Pelecanoides urinatrix, South-Georgian diving petrel P. georgicus, blue petrel Halobaena caerulea). These studies showed evidences for nestand partner-odour recognition in procellariid seabirds, which provide an olfactory signature that allows birds to recognize their own burrow. We can therefore be reasonably confident that our results actually reveal that P. pacificus can detect but do not avoid the odour of ship rats in our study area.

This absence of avoidance is counter-intuitive, especially in light of the extensive use of olfaction in procellariid seabirds for various purposes [START_REF] Warham | The Behaviour, Population Biology and Physiology of the Petrels[END_REF]. Although the use of olfaction to assess predation risk has never been tested in procellariid seabirds, recent studies with hole-nesting songbirds have shown some evidence of variation in the ability to detect predators between closely related species [START_REF] Johnson | Lack of predator-odor detection and avoidance by a songbird, the House Wren[END_REF]. Naïve great tits (Parus major) (i.e. main-tained in captivity for 10 days after hatching and without predation events or signs of predator visits to nest boxes containing nestlings during the first 10 days of their life) avoided the odour of predators when selecting cavities for roosting [START_REF] Amo | Smelling out predators is innate in birds[END_REF]. However, eastern bluebirds (Sialia sialis), which had evolved with snakes and small mammal predators, were as likely to lay eggs in boxes with predator cues as in boxes with neutral cues [START_REF] Godard | Eastern bluebirds Sialia sialis do not avoid nest boxes with chemical cues from two common nest predators[END_REF]; and house wrens (Troglodytes aedon), another species which had co-evolved with nest predators, either did not detect or did not respond to nest predator odour [START_REF] Johnson | Lack of predator-odor detection and avoidance by a songbird, the House Wren[END_REF]. Two native bird species from New Zealand, the rifleman (Acanthisitta chloris) and the South Island robin (Petroica australis), which had not co-evolved with any mammalian predators, did not change their behaviour at nests when the odour of the ship rat (also an introduced predator in New Zealand) was present. In the same study area, only one of the two introduced European passerines, which had co-evolved with mammalian predators, altered their behaviour to minimize risk to themselves [START_REF] Stanbury | I smell a rat: can New Zealand birds recognize the odor of an invasive mammalian predator?[END_REF]. In our study, the lack of co-evolution with mammalian predators combined with the presence of two different introduced rat species, respectively for about 3000 and 150 years, apparently did not lead to development of, or variation in, anti-predator behaviour in P. pacificus.

Following the introduction of a new predator in an ecosystem, it has been shown that some species of amphibians and mammals can rapidly develop antipredator responses [START_REF] Kiesecker | Population differences in responses of red-legged frogs (Rana Aurora) to introduced bullfrogs[END_REF][START_REF] Russell | Do Australian small mammals respond to native and introduced predator odours?[END_REF]. Regarding birds, one study showed that the New Zealand bellbird (Anthornis melanura) was able to respond to nest predation risk after a co-existence of about 700 years with introduced predators (i.e. mustelids, rats, cats, possums, hedgehogs) [START_REF] Massaro | Introduced mammalian predators induce behavioural changes in parental care in an endemic New Zealand Bird[END_REF]. No data are available on the time that seabirds need to adapt their behaviour, and the about 150 years of co-existence between shearwaters and ship rats in our system may not be long enough to induce behavioural adaptations. The presence of a predator archetype (i.e. predator species that use similar morphological and behavioural adaptations in obtaining prey) might favour an antipredator response from island prey [START_REF] Cox | Naivete and an aquatic-terrestrial dichotomy in the effects of introduced predators[END_REF]. Here, however, the roughly 3000-year presence of the Pacific rat, belonging to the same predator archetype as the ship rat and having similar effects on seabirds weighing <300 g [START_REF] Towns | Eradications as reverse invasions: lessons from Pacific rat (Rattus exulans) removals on New Zealand islands[END_REF], did not prepare shearwaters to avoid the odour of the ship rat.

Procellariiforms such as P. pacificus are highly philopatric and highly faithful to their breeding site [START_REF] Warham | The Petrels:Their Ecology and Breeding Systems[END_REF]). These birds form long-term pair bonds, and site fidelity constitutes a means for pairs to reunite [START_REF] Bried | Mate fidelity in monogamous birds: a re-examination of the Procellariiformes[END_REF]. These biological character- istics may thus strongly constrain breeding site selection and encourage birds to come to breed on the same sites, despite the detection and presence of rats. Shearwaters may also rely on cues other than smell to ascertain the presence of ship rats. These birds could use visual cues (i.e. direct encounters with rats) to assess the risks of nesting in a colony. Another cue might be conspecific reproductive success [START_REF] Danchin | Conspecific reproductive success and breeding habitat selection: implications for the study of coloniality[END_REF]. The long-lived shearwaters typically spend their first 3-5 years as non-breeders but regularly prospect colonies, and in so doing are able to assess average breeding success in different colonies so as to choose the most successful breeding site [START_REF] Warham | The Petrels:Their Ecology and Breeding Systems[END_REF][START_REF] Warham | The Behaviour, Population Biology and Physiology of the Petrels[END_REF][START_REF] Danchin | Conspecific reproductive success and breeding habitat selection: implications for the study of coloniality[END_REF]. Breeding site selection based on an integrative cue such as conspecific reproductive success is likely to be more efficient than direct cues of the presence of predators.

All these factors may well explain the absence of avoidance of the ship rat odour; yet, some observations had led us to believe that P. pacificus would respond. In fact, the dramatic increase in some shearwaters' breeding population immediately following rat eradication [START_REF] Bourgeois | Dramatic increase in the Zembretta Yelkouan shearwater breeding population following ship rat eradication spurs interest in managing a 1500-year old invasion[END_REF][START_REF] Vanderwerf | Response of wedge-tailed shearwaters (Puffinus pacificus) to eradication of black rats (Rattus rattus) from Moku'auia Island after reinvasion[END_REF][START_REF] Vanderwerf | Increase in wedge-tailed shearwaters and changes in soil nutrients following removal of alien mammalian predators and nitrogen-fixing plants at Kaena Point[END_REF]) suggested that procellariid seabirds may select their breeding sites according to direct cues. However, we hypothesized that this selection could also be at least partially driven by olfaction (avoidance of burrows 'smelling' of rats), with a predation risk assessment based upon predator chemical cues. Moreover, there is growing evidence that some shearwater species select breeding areas based on the absence of introduced predators, like ship rats, at different spatial scales [START_REF] Bourgeois | Yelkouan shearwater nest-cavity selection and breeding success[END_REF][START_REF] Ruffino | Introduced predators and cavity-nesting seabirds: unexpected low level of interaction at breeding sites[END_REF][START_REF] Ruffino | Invasive rats and seabirds after 2,000 years of an unwanted coexistence on Mediterranean islands[END_REF]. For example, at the nest scale, the yelkouan shearwater (Puffinus yelkouan) avoids cavities frequented by rats and preferentially selects the deepest and most winding cavities for breeding [START_REF] Bourgeois | Yelkouan shearwater nest-cavity selection and breeding success[END_REF][START_REF] Ruffino | Introduced predators and cavity-nesting seabirds: unexpected low level of interaction at breeding sites[END_REF]. At the colony scale, selection of intra-island refuges (e.g. steep cliffs) less accessible to mammal predators could also partly explain the surprising length of apparent coexistence (about 2000 years) between procellariid seabirds and invasive ship rats on Mediterranean islands [START_REF] Ruffino | Invasive rats and seabirds after 2,000 years of an unwanted coexistence on Mediterranean islands[END_REF].

Although [START_REF] Smith | Recovery of native species following rat eradication on Mokoli'i Island, O'ahu, Hawai'i[END_REF] has shown that the ship rat could dramatically reduce the breeding success of P. pacificus, we suspect that for our three studied New Caledonian islets, the impact (i.e. the level of predation on eggs or chicks) of the ship rat may not actually be great enough to induce avoidance behaviour. In fact, if the costs of antipredator responses do not outweigh the benefits, natural selection may not favour the detection of predator chemical cues, nor favour individuals that respond to this odour [START_REF] Amo | Smelling out predators is innate in birds[END_REF]. The limited impact of ship rats may be explained by the presence of alternative food resources or may reflect the process by which these predators were introduced. On islands, rats are likely to be introduced in an isolated manner, a few individuals at a time, which may result in a population that does not necessarily impact seabirds. Rat density [START_REF] Igual | Rat control and breeding performance in Cory's shearwater (Calonectris diomedea): effects of poisoning effort and habitat features[END_REF]) and factors intrinsic to rats such as physical-limiting factors [START_REF] Freeman | Measuring bite force in small mammals with a piezo-resistive sensor[END_REF][START_REF] Williams | Gape and bite force in the rodents Onychomys leucogaster and Peromyscus maniculatus: does jaw-muscle anatomy predict performance?[END_REF][START_REF] Zarzoso-Lacoste | Limited predatory capacity of introduced black rats on bird eggs: an experimental approach[END_REF], lack of predation skill or social learning [START_REF] Grant | Rat predation on Bonin petrel eggs on Midway atoll[END_REF][START_REF] Booth | Kiore (Rattus exulans) predation on the eggs of the Little Shearwater (Puffinus assimilis haurakiensis)[END_REF] can alter the magnitude of rat impact on seabirds. Therefore, further experiments should be conducted on a variety of procellariid seabirds, prospecting or breeding birds, and within colonies where the impact of rats is quantified, to determine to what extent ecological factors, bird species characteristics (e.g. body mass, egg size; [START_REF] Bradley | Rodents as nest predators: influence on predatory behavior and consequences to nesting birds[END_REF][START_REF] Jones | Severity of the effects of invasive rats on seabirds: a global review[END_REF][START_REF] Towns | Eradications as reverse invasions: lessons from Pacific rat (Rattus exulans) removals on New Zealand islands[END_REF], reproductive status of individuals and intensity of predator's impact influence the onset of anti-predator behaviour in procellariid seabirds.

Fig. 1 .

 1 Fig. 1. Diagram of the Y-maze used for experiments.

Fig. 2 .

 2 Fig. 2.Avoidance rating (i.e. number of unscented arm choices divided by total number of arm choices) of birds for arm treated with predator (Rattus rattus) odour on the three islets of Isle of Pines Archipelago (New Caledonia). The dotted line indicates the rating fixed for no effect of odour, 50%. The species of rat present on the islets is indicated under A, B and C.

Table 1 .

 1 Results of generalized linear model for avoidance rating of arm treated with predator odour as compared with no effect of odour (avoidance rating 50%) for the three islets and for the two islets with ship rats (i.e. invaded) and the islet without ship rats (i.e. non-invaded)

			Standard		Pr
		Estimate	error	z value	(>|z|)
	Islet A	0.04	0.30	0.15	0.88
	Islet B	-0.13	0.52	-0.26	0.80
	Islet C	0.30	0.32	0.94	0.34
	Invaded (A + B)	0.00	0.26	0.00	1.00
	Non-invaded (C)	0.30	0.32	0.94	0.34

© 2015 Ecological Society of Australia doi:10.1111/aec.12252

A. GÉRARD ET AL. © 2015 Ecological Society of Australia doi:10.1111/aec.12252

ACKNOWLEDGEMENTS

We thank the traditional and civil authorities of Isle of Pines and Province Sud for allowing us access to the field sites. We are grateful to H. Kouate, E. Muret and L. Debar, for their help in the field, to K. Bourgeois for its scientific advice and to M. Sweetko for English language revision. A.G. was funded by a Ph.D. scholarship from the École Doctorale Sciences de l'Environnement EDSE251. Additional funds were provided by Province Sud (DENV). We thank the two anonymous reviewers and editor for constructive comments on a draft of this manuscript. The experiments comply with the current laws of France and New Caledonia (permission for sampling protocol n°2155-2012/ARR/DENV).