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Popul Ecol (2008) 50:91100 DOI 10.

1007/s10144-007-0059-z

ORIGINAL ARTICLE

Effects of anthropogenic food resources on yellow-legged gull colony size on Mediterranean islands
line Duhem Philip Roche Eric Vidal Ce Thierry Tatoni

Received: 28 December 2006 / Accepted: 3 July 2007 / Published online: 21 August 2007 The Society of Population Ecology and Springer 2007

Abstract Yellow-legged gull Larus michahellis populations have been studied on three archipelagos consisting of 20 islands distributed along 80 km of the French Mediterranean coastline. Population changes were analyzed between 1920 and 2006. In the rst decades following their settlement on these islands, the yellow-legged gull populations showed a continuous exponential growth in the three archipelagos, in agreement with an annual geometric growth rate k above 1. The population growth ceased to t this model during the 1980s for the older colonies (Riou ` res Islands archipelagos). Thus, we focused on and Hye population changes occurring during the period 1982 2000, a pivotal period for which we have both precise census and anthropogenic food resource data, in order to determine environmental factors inuencing these population changes using multiple linear regression models. An average annual growth rate of colony size was 1.02 for the last two decades. The changes in landll availability, the gull density in 1982, and the nesting area in 1982 explained 84.4% of variation in colony size changes between 1982 and 2000. The yellow-legged gull changes on the islands in the last two decades increased as availability in anthropogenic food resources increased near the colony (positive DK). As a consequence, given no reduction in landll

activity or in accessibility for gulls, we expect this region to sustain continuous species expansion in the future. Keywords History of colonization Landll Mediterranean rocky islands Urbanization

Introduction The factors determining population size changes are of central interest for both the conservation of threatened species and the population regulation of species whose high number of individuals sometimes results in negative interactions with biodiversity and/or human interests. In the case of colonial seabirds, both cases can be found. In particular, large gull species are extremely similar in terms of ecology and behavior, and thus their population sizes are the main factors determining their classication as threatened or not. Several large gull species are opportunistic feeders and are able to forage on anthropogenic food resources, such as trawling discards or domestic refuse on landlls (e.g., Mudge and Ferns 1982; Chudzik et al. 1994; Pierotti and Annett 1990, 1991). For these species, the presence, abundance, and nature of anthropogenic food resources often determine the choice of nesting sites (Scarton and Valle 1996); the spatial distribution of gulls during both the breeding season and winter (Fasola and Canova 1992; Sol et al. 1995); their diet (Belant et al. 1993; Bosch et al. 1994; Oro et al. 1995); and their nska et al. 1996; Oro et al. reproductive parameters (Bukac 2004). Thus, a high availability of anthropogenic food resources often leads to an increase in recruitment rates, notably because of a probable decrease in winter mortality of the youngest gulls, as well as signicantly higher reproductive success (Pons and Migot 1995; Brousseau

C. Duhem (&) P. Roche E. Vidal T. Tatoni diterrane en dEcologie et de Pale oe cologie Institut Me Paul Ce zanne (IMEP-CNRS-UMR 6116), Universite timent Villemin, (Aix-Marseille III), Ba Domaine du Petit Arbois, Avenue Philibert, BP 80, 13545 Aix-en-Provence, Cedex 04, France e-mail: celine.duhem@univ-cezanne.fr P. Roche EMAX, 3275 Route de Ce zanne, CEMAGREF, Unite CS 40061, 13182 Aix-en-Provence, Cedex 5, France

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et al. 1996). In turn, a decrease in anthropogenic food availability is correlated with an increase in the probability of permanent emigration (Oro et al. 2004). During the past few decades, several large gull species have undergone a large increase in abundance, especially in Europe (e.g., Spaans and Blokpoel 1991) and North America (e.g., Blokpoel and Spaans 1991). Whereas certain studies have addressed the effects of food availability and protection status on population size changes in threatened gull species such as Audouins gull, Larus audouinii, (Martinez-Abrain et al. 2003; Oro et al. 2004), no study examines this topic for large, nonthreatened gull species currently undergoing population expansion. Yellow-legged gull, Larus michahellis, populations have markedly increased in population size over the past 50 years (e.g., Thibault et al. 1996), especially along the northern shore of the Mediterranean Sea, where 120,000 rennou et al. 1996). nesting pairs have been recorded (Pe These populations are still increasing (BirdLife International 2000) and are considered as problematic given their negative interactions with human activities and other wild species. The latter include changes in island vegetation and terrestrial insect assemblages (Vidal et al. 1998; Orgeas et al. 2003). Negative effects on waterbirds have also been reported but are still under debate (Oro and MartinezAbrain 2007). Previous studies have shown that this species feeds on both trawling discards and landlls (Bosch et al. 1994; Sol et al. 1995; Gonzalez-Solis 2003). In contrast to trawling activities, landlls provide highly predictable food resources because they are daily and locally abundant throughout the year (e.g., Burger and Gochfeld 1983; Horton et al. 1983). This particularity may inuence the distribution and population size changes for species that depend on landlls as their primary food resource, such as the yellow-legged gull along the French Mediterranean coast (Duhem et al. 2003a, b; 2005). Generally, the three suspected determinants for the strong population increase of several large gull species throughout the Palearctic during the past few decades were the legal protection of the species, the protection of the potential breeding sites, and the increasing availability of articial food resources (i.e., refuse in landlls or trawling discards; e.g., Spaans and Blokpoel 1991). The heterogeneous spatial distribution of anthropogenic foraging habitats (landlls) on the mainland and the availability of potential breeding sites (coastal islands) along the French Mediterranean coast, in addition to their differential degree of protection status, constitute a good model to determine the main factors inuencing yellow-legged gull population size changes. Thus, we tested the hypothesis that resource availability, especially changes in landll accessibility and domestic refuse abundance, would be the most important

explanatory factor of population size change for the yellow-legged gull compared with the topography and protection status of breeding sites. In this study, we analyzed the contribution of these variables to changes in population size observed between 1982 and 2000 on 20 island colonies.

Materials and methods Study sites We carried out this study on 20 islands distributed primarily among three archipelagos and along 80 km of the French Mediterranean coastline (Fig. 1). The western islands are limestone with scarce scrublands, providing

N FRANCE O S E

Marseille

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=1.12
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=0.99
15 13 16 14 18 19 0 2km 17 20

: 1.06-1.19

:1.01-1.05

=1

<1

Fig. 1 Map of the study area (southeast France) showing the location of the 20 islands censused (numbered 120, see Appendix for name and islands details) and landll locations. The changes in colony size and density between 1982 and 2000 are indicated on each site studied. Colony size is shown using circles, which vary in size according to the number of yellow-legged gull pairs censused in 2000, and variation in grayscale indicates the changes of the colony size (points k < 1, white k = 1, grey 1.01 < k < 1.06, dark k  1.07). Landll in use before 1982 Landll in use after 1982 Coastal town > 50,000 inhabitants

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suitable nesting sites over roughly the total island area. In contrast, the eastern islands are granitic with dense vegetation, and nesting sites are generally restricted to the coastal belt and any other poorly vegetated areas. Due to these differences, total island area does not necessarily represent nesting area. Thus, to determine the nesting area (ha), we delineated nesting areas on aerial photographs using ArcGis 8.0 and eld-collected nesting data in 1982 and 2000. The yellow-legged gull is known to move up to 40 km from its colony to forage (Witt et al. 1981; Oro et al. 1995). Within this optimal foraging range, we identied ten large landlls that were all actively used as foraging sites by yellow-legged gulls (ca. a minimum of 7,000 gulls per day and per site; Duhem 2004). These landlls all handle more than 70,000 tons per year of the same refuse type (i.e., mainly domestic waste; ADEME 2000), and they are all managed in the same way: refuse is covered every evening, and no pest control occurs. Landlls occur mainly in the western part of the study area, near Marseilles city, which is responsible for a strong landll accessibility gradient, decreasing from west to east (Fig. 1).

growth patterns in our area, i.e., 19822000. Between these two dates, population changes ceased to t the exponential growth model, whereas new colonies in the Frioul archipelago islands, settled since 1977 (Launay 1983), showed a marked increase in size. During this pivotal period, two precise censuses were performed on 20 rocky islands in 1982 (Vidal 1982; Launay 1983) and in 2000 (Duhem et al. 2008). In addition, we also have precise estimates of landll food resource availability for these years (Duhem 2004). Between these 2 years, we calculated k for 20 rocky islands with permanent colonies of yellow-legged gulls using the formula proposed by Migot and Linard (1984) and Bosch et al. (2000), as the regression method is not meaningful using two points only. k Nt =N0 1=t 1

t is the number of years between two subsequent censuses, and N is the number of breeding pairs in 1982 (N0) and 2000 (Nt). In order to obtain standard error estimates for this parameter, we used the census accuracies as an error assessment and propagated it to the computation of k (Goodman 1960; Ku 1966). The standard error of k can be estimated from the standard error of Nt/N0 following Eq. 2: sNt =N0 sk 1=t Nt =N0 2

Colony size and population changes Colony sizes of breeding yellow-legged gulls have been available since the 1920s for the three archipelagos (Heim de Balzac 1923; Launay 1983). Using these data, we assessed the population changes for each archipelago since 1920 by estimating k, the mean annual geometric growth rate of a population. The growth rate (k) was estimated by a generalized linear model (GLM) regression analysis of the number of breeding pairs with time. The exponent of the regression slope and its 95% condence intervals (CI) corresponded to the population growth rate k and its CI. This method is suitable because it is robust to both stochastic environments and census errors and allows for unequal time census intervals (Oro and Martinez-Abrain 2007). Since 1982, censuses of yellow-legged gull colonies have been based on two complementary techniques traditionally used for seabird populations (Bibby et al. 1992; Komdeur et al. 1992), thus providing more precise data and allowing comparison among them (the 1989 census was excluded because it was a global assessment of colony size at the archipelago level; Vidal et al. 2004). For accessible colonies, a marker was deposited in each individually counted nest. For inaccessible sites, this approach was replaced by a remote census from a topographic peak or from a boat, using binoculars. Visibly incubating birds, as well as individuals stationed in pairs, were counted (Bibby et al. 1992). In order to study the determinants of population change, we focused on a pivotal period for the population

sNt =N0 is the standard error of the ratio of the 2000 to 1982 numbers of breeding pairs censused, t is the number of years between the two subsequent censuses. sNt =N0 was computed using Eq. 3, as proposed by Ku (1966): sNt =N0 Nt N0 s s2 s2 N0 Nt N0 2 Nt 2 3

sN0 and sNt were estimated using an accuracy estimate of 5% for the breeding pair censuses. Based on the standard error estimate of k, we tested its signicance under the hypothesis of no change in time (k = 0) and using the Normal law.

Environmental variables We considered 26 environmental variables that could be clustered into ve main groups: (1) island topography, (2) yellow-legged gull colonization history, (3) colony status, (4) island disturbance by human activities, and (5) anthropogenic food availability in the species foraging range. These variables were chosen because they can potentially inuence spatial distribution, size, and density of yellow-legged gull colonies (Fasola and Canova 1992; Goutner 1992; Scarton and Valle 1996; Bosch and Sol

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1998). As this number of variables is quite high compared with the number of sites, we used a principal component analysis (PCA) in order to identify the most correlated variables and reduce the number of variables to ten previous to regression analysis. These retained variables belong to four groups: (i) island topography as described by (1) elevation (m), and (2) isolation (m), (ii) the colonization history in the study area including (3) the distance from the initial site of colonization, i.e., Riou island (DInitial colony; m), and (4) the age of each colony (years), (iii) the colony status as determined by (5), the nesting area (ha) used in 1982 (na82), (6) the density of the colony in 1982, and (7) S82, the ratio between na82 and the total island area, and nally (iv) the anthropogenic food availability described by (8) Ton, the annual tonnage in 1982 of the nearest landll, (9) DDmin the change, between 1982 and 2000, in the minimum distance to a landll, and (10) DK the change in K (the ratio between the annual tonnage of the nearest landll and its distance to the colony).

Data analysis We used multiple linear regressions to model changes in colony size of the yellow-legged gull. A high number of explanatory variables relative to sample size generally causes overtting in multiple linear regression (MLR). In order to identify the most important explanatory variables, we used the best subset method; all potential MLR models starting from one variable to ten variables were tted sequentially and independently (Montgomery and Peck 1982). We searched for the most parsimonious models (with the smallest number of variables) having a strong explanative power as dened using criteria parameters: the adjusted R2, the Mallows Cp coefcient (Mallow 1973), and the residual variance. Contrary to the R2, the adjusted R2 does not always increase with the number of variables. The Mallows Cp coefcient measures the efciency of each subset model relative to the full model. In the case of least square regression, the Mallows Cp is equivalent to Akaike information criterion (AIC), which is more devoted to maximum likelihood models. The best model should have a small Mallows Cp, a high adjusted R2, and a low residual variance. A Cp value (lower or close to the number of regression parameters including the intercept) indicates that the there is no signicant bias in the model due to variable redundancy. It is common for the best subset methods to identify several potential models. In order to avoid arbitrarily choosing one model, we chose to examine the best three models (hereafter called concurrent models). For these three models, a full multiple linear regression (MLR) was computed, and we used additive diagnostic checks of the statistical properties to identify the best one.

Collinearity among variables is a common issue with environmental variables. We used the variance ination factor (VIF) to deal with this problem. The VIF measures how much the variance of an estimated regression coefcient increases when other correlated variables are included in the model. Montgomery and Peck (1982) suggest that if the VIF is >5, the regression coefcients are poorly estimated. Thus, we considered only models with variables that have VIF <5. The DurbinWatson statistic was used to check for the presence of autocorrelation in regression residuals. Residual distributions were visually checked to identify variance patterns and normality. Potential outliers were identied using Studentized residuals. Finally, the R2 calculated from predicted residual sum of squares (PRESS) (hereafter called predicted R2) was used to estimate the predictive power of the regression model. Predicted R2 can prevent overtting the model and is more useful than adjusted R2 for comparing models because it allows assessment of the predictive power for individual values not included in the model. When the predicted R2 is close to the adjusted R2, it suggests that the model has a good predictive ability and is robust to omission of some observations. We tested for an island protection status effect on yellow-legged gull population changes (Table 1). The protection status was coded into three groups: (A) no protection status, (B) protected and restricted access acquired in the 1990s, and (C) protected and restricted access to colonies acquired before 1982. Protection status refers to inclusion in a national park or natural reserve or territory acquired by the Conservatoire du Littoral. All three situations involve environmental management of the island mainly through limitation of human disturbance. Restricted access refers either to military sites or to nature reserves where human access is strictly forbidden and only natural processes are present in the ecosystem. As the number of islands in these groups is low, we used a nonparametric median comparison test, Moods median test, which is a nonparametric analog of a one-way analysis of variance (ANOVA). We tested the hypothesis of no median k differences between the groups for colony size changes according to protection status. All the computations were done using the MINITAB 14 package ( 19722004 Minitab)

Results Population changes between 1920 and 2006 (archipelago level) In the rst decades following their settlement on islands, the yellow-legged gull populations had a signicantly

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Table 1 Results of the censuses performed in 1982 and 2000 on 20 islands and islets of the French Mediterranean shore and the derived annual growth rates of colony sizes, k, between 1982 and 2000 and their standard errors Islands and islets Protection status Number of breeding pairs 1982 589 A A A B B B B B B B A A A C C C A C C C 304 265 20 8,750 6,000 800 800 1,000 60 80 10 5 15 5,225 1,515 2,255 450 650 130 65 40 120 2000 4,323 1,799 2,449 75 11,891 6,111 1604 1845 1,965 119 223 24 113 98 4,299 1,275 1,343 619 667 150 104 38 103 k 1.117 1.104 1.131 1.076 1.017 1.001 1.039 1.048 1.038 1.039 1.059 1.050 1.189 1.110 0.989 0.990 0.972 1.018 1.001 1.008 1.026 0.997 0.992 sk 0.0002 0.0003 0.0002 0.0005 0.0015 0.0020 0.0010 0.0009 0.0010 0.0010 0.0007 0.0008 0.0001 0.0003 0.0024 0.0024 0.0034 0.0015 0.0020 0.0017 0.0013 0.0021 0.0023 * * * * * * * * * * * * * * * Difference in annual growth * * * * *

Frioul archipelago Ratonneau ` gues Pome Tiboulen de Ratonneau Riou archipelago Riou re Ma Jarre et Jarron Plane re Tiboulen de Ma Grand Congloue Petit Congloue Verte Grand Rouveau ` res Islands archipelago Hye Porquerolles Le Levant Port-Cros Bagaud Grand Ribaud ` re Gabinie Petit Langoustier Gros Sarranier

Islands and islets are listed according to their archipelago following a westeast distribution A no protection status, B protected and restricted access acquired in the 1990s, C protected and restricted access to colonies acquired before 1982 *Annual growth signicantly different from 1 (null population change in time) at the risk of 5%

continuous exponential growth in the three archipelagos, in agreement with an annual geometric growth rate k above 1 ` res island (Fig. 2). For the populations of the Riou and Hye archipelagos, the population increase t with an exponential growth model for 19201982, with an annual estimated growth rate of 1.061 (CI 0.006) and 1.049 (CI 0.002), respectively. For the Frioul archipelago, in keeping with the rst settlement of yellow-legged gulls on the Frioul archipelago in 1977, the population increase t with an exponential growth model for the period 19772006, with an estimated growth rate of 1.102 (CI 0.011). Exponential population growth is always transient, as it requires unlimited resources. The populations ceased to t the exponential growth model during the 1980s for the ` res Islands archipelagos). older colonies (Riou and Hye ` res Islands archipelago had a During the 1980s, the Hye population peak between 1982 and 1989, with 5,502 and 5,732 pairs, respectively. After this period and between 1989 and 2006, the population decreased at an annual rate

of k = 0.983 (CI 0.008). For the Riou archipelago, the population growth rate slowed down to k = 1.019 (CI 0.003) between 1982 and 2006. For the Frioul archipelago colonies, which were settled three decades ago, population growth still ts the exponential growth model.

19822000: the pivotal period of population change Based on the census estimates of breeding pair numbers for 20 islands and islets, we calculated an annual growth rate k at the archipelago and island level (Table 1). Based on the error sampling rate, the standard error of the annual growth rate was computed and used to test it against the hypothesis of a null growth rate. At the scale of the studied region, variability in growth rate existed both at the archipelago ` res archipelago populations and island levels. The Hye signicantly decreased, whereas the Riou and particularly the Frioul populations continued to signicantly increase

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(Table 1; Fig. 2). All three islands of the Frioul archipelago had a signicant population increase during this period, ` gues island, with a mean annual the highest being Pome population increase of 1.131. For the Riou archipelago, all islands had signicant population increases with the exception of Riou island, which had a quite stable colony size during this period (Table 1). The highest increase was island. Intermediate 1.059 per year for the Grand Congloue islands (Verte and Grand Rouveau), located between Riou ` res island archipelagos, had signicant and high and Hye ` res annual growth rates (1.189 and 1.110). For the Hye Islands archipelago, the population decrease of 1.1% (0.989) per year between 1982 and 2000 was signicant using the error propagation approach. At the island level, some islands had signicantly decreasing populations (Porquerolles, Le Levant, and Gros Sarranier) or had quite stable populations (Bagaud and Petit Langoustier), whereas others had signicantly increasing populations (Grand Ri` re). baud, Port-Cros, and Gabinie

variables. The selected variables were DK, GullDens82, and na82 (see Appendix for actual values). The three variables had signicant regression coefcients and VIF values below 1.2 (Table 2), indicating very low collinearity between variables. The DurbinWatson statistic (2.14) and the distribution patterns of coefcients indicated no evidence of autocorrelation between residuals and residual normality. The regression model has the form: k 0:626 0:465 DK 0:00046 GullDens82 0:000645 na82 This means that for colonies with the strongest increase in colony size over the last 20 years, the increase occurred on islands with low gull density and limited nesting area in 1982, for which the availability of anthropogenic food resources had increased during this period either due to the settlement of landlls nearer the colony or to an increase in the annual refuse tonnage of the nearest landll. The predictive value of the model appeared to remain high, with a predicted-R2 value of 77.81%, indicating that the model was stable. Moods median test for island protection status effects indicated a signicant difference in colony size changes between the groups (chi-square = 8.57; df = 2; P = 0.014). Visual examination of a box plot per status group (Fig. 3) indicated that colony size changes were lower when the protection status increased (A > B > C). Discussion At the Mediterranean basin level, yellow-legged gull populations have greatly increased, with an average growth rate of around 79% per year over the past 50 years (Thibault et al. 1996). In our study area, the populations
Table 2 Regression coefcient estimates and standard errors for yellow-legged gull population dynamics from the multiple linear regression model with three variables Variable Intercept Estimate 0.626 0.465 4.56 104 6.45 104 Standard error 7.40 102 7.09 102 1.17 104 1.76 104 t 8.46 6.55 3.90 3.65 P 0.000 0.000 0.001 0.002 1.2 1.2 1.1 VIF

Causes of change in colony size between 1982 and 2000 The best subset procedure allowed us to examine three concurrent models with adjusted R2 values of 84.4% (three variables), 85.8% (four variables), and 86.4% (ve variables), respectively. The Mallows Cp coefcients were all low (1.35, 1.38, and 2.16, respectively). Given the very low increments of the determination coefcient with the increase of variables and the fact that the three variables included in the rst model were also included in the two others, we retained the most parsimonious model with three
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Student t values and P values are used to assess the signicance of estimates
Dat e

The variance ination factor (VIF) measures how much the variance of an estimated regression coefcient increases if variables are correlated (VIF < 5 indicates a null or low collinearity of variables) DK change in the ratio between the annual refuse tonnage in and the distance to the nearest landll between 1982 and 2000, GullDens82 breeding gull density in 1982 (pairs/ha), na82 the nesting area (ha) in 1982

Fig. 2 Yellow-legged gull population changes from 19202006 in the three archipelagos of the French Mediterranean (number of nesting pairs). The focus period (19822000) is highlighted by the grey rectangle

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Protection Status
Fig. 3 Box plot of changes in colony size from 19822000 per protection status group for the 20 rocky islands of the French Mediterranean shore. A no protection status, B protected and restricted access acquired in the 1990s, C protected and restricted access to colonies acquired before 1982.

also increased between 1953 and 1982, with a growth rate of 9% per year (Vidal et al. 2004; this study). A large change occurred in this pattern of increase in the 1980s. After 1982, the yellow-legged gull population increase did not t with exponential growth for the older colonies (Riou ` res Islands archipelagos), whereas the populations and Hye that were newly settled on the Frioul archipelago had exponential growth. Based on these results, 19822000 seems to be a pivot point for the population growth of this species in the area. Currently, the yellow-legged gull populations appear to be still expanding but at a reduced speed, with an average growth rate of 2% per year (Oro and Martinez-Abrain 2007; this study). Some colonies have probably reached their equilibrium size, such as those at Riou island, the species initial site of settlement in France (Jaubert and Lapommeraye 1859; Heim de Balzac 1923), which shows a null growth rate between 1982 and 2000. Our results conrm the importance of anthropogenic food resource availability for yellow-legged gull population changes since 1982. The populations increased as availability in anthropogenic food resources increased near the colony (positive DK). This can be due to the opening of a new landll near the colony or the increase in refuse tonnage in the nearest landll, or both. The changes in colony size followed the same trend as the anthropogenic food resource availability during the last two decades. From the 1980s, the quantity of domestic waste produced increased by 5.7% per year between 1982 and 1993, then by 1.3% per year between 1993 and 2000 (ADEME 2000). The rst landlls opened in our study area in 1974, when nine yellow-legged gull colonies were already present among the 20 islands under consideration. The 11 remaining islands were colonized between 1974 and 1983

(Appendix). During the 18-year period examined in our study, anthropogenic food resource availability increased in the vicinity of colonies, with the exception of the col` res Islands archipelago. Indeed, in onies settled on the Hye 1984, the construction of an incinerator in Toulon city caused a drop in the annual refuse tonnage of the nearest landll for these colonies (Fig. 1). These islands were exceptional in that they decreased in colony size during the study period despite having had strong protection status since 1963 (National Park). Nevertheless, anthropogenic food resource availability cannot solely explain the spatial variability of yellow-legged gull population changes. Breeding site selection by colonial seabirds is generally the consequence of the previous years breeding success (Danchin et al. 1998), or linked with the presence of conspecics (Oro and Pradel 2000; Oro and Ruxton 2001), or both (Brown et al. 1990, 2000). In a recent study on recruitment in expanding gull populations, Oro and Pradel (2000) demonstrate that local recruitment and colony size are linked. However, colony expansion causes increasing resource competition, thus decreasing the probability of recruitment to the local population after a given threshold, making the founding of a new colony an increasingly attractive strategy (Forbes and Kaiser 1994; Oro and Ruxton 2001). The fact that a small nesting area favored an increase in colony size may correspond to the colonization of small islets subsequent to saturation of nearby larger islands. Due to the archipelago structure, the distance between large islands is greater than that separating large islands from islets (Forbes et al. 2000). Therefore, the colonization of the nearest sites by breeding gulls implies that these low-elevation and low-area islands house relatively large and dense colonies (limited by the island area). In addition, islets are less disturbed by human activities (such as tourism), and in the case of the granitic sites, islets are the only sites where the vegetation cover is less dense, thus allowing the settlement of relatively large (several tens of pairs) and aggregated colonies. The yellow-legged gull had protected status throughout the European Union from 1981 (Annex II bird species of the Bird Directive 79/409/CEE). It is interesting to note that the strong demographic increase within the species in Europe occurred while it was not yet protected either by the Bird Directive (79/409/CEE) or French laws. We did not interpret this observation in a causal way. We only considered that the protection status of the species did not induce a population increase. We also tested for a protection status effect among the colonies. Our results indicated the opposite effect to that which we were expecting, i.e., the better-protected colonies were the ones with decreasing population changes and vice versa. Again, care must be taken when interpreting this result, because protection status certainly does not induce a decrease in population

Colony size change ()

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variables. Considering individual colonies leads us to suggest that an interaction between protection status and breeding site characteristics is more likely to be responsible for the patterns found. Most of the limestone islands have characteristics known to be typical of gull breeding sites: a large area allowing the settlement of large colonies, a patchy matorral vegetation providing considerable shelter and good visibility, and a lack of urbanization (e.g., Scarton and Valle 1996; Bosch and Sol 1998; Kim and Monaghan 2005). Access to these islands is forbidden or has been recently restricted. These islands have no or recently restricted access. In contrast, the granitic islands have a dense vegetation cover that prevents nesting throughout most of the area, despite high levels of protection. Thus, as for the protection of the species, the protection of the colonies did not appear to be a signicant factor in explaining yellow-legged gull population size changes. In a recent study, Martinez-Abrain et al. (2003) came to the same conclusion for the Audouins gull. In conclusion, our results showed that anthropogenic food availability has strongly inuenced the recent local population changes of the yellow-legged gull on the rocky islands of the French Mediterranean coast. These results agree with the results of Oro et al. (2004) dealing with the Audouins gull population changes and trawling discard availability. Unlike trawling activity, landlls provide a Appendix
Table 3 Topographic features of the 20 islands and islets examined in the study (see Fig. 1 for locations) and environmental variables retained by the multiple linear regression Islands and islets Tiboulen de Ratonneau Ratonneau ` gues Pome re Tiboulen de Ma re Ma Jarre - Jarron Plane Riou Petit Congloue Grand Congloue Verte Grand Rouveau Grand Ribaud Petit Langoustier GullDens82 breeding gull density in 1982 (pairs/ha), na82 nesting area (ha) in 1982, DK change in the ratio between the annual refuse tonnage in and the distance to the nearest landll between 1982 and 2000 Porquerolles Gros Sarranier Bagaud ` re Gabinie Port-Cros Le Levant

constant supply of food resources, and we can predict that, in view of the current urbanization trend on the mainland, human activities will cause an increase in annual refuse tonnages if changes in refuse management are not implemented (e.g., closing landlls or replacing them by incinerators). In addition, the small gull density of some large islands (Duhem et al. 2008), in addition to the potential breeding habitat provided by cities surrounding the older colonies, implies that there are probably nesting sites available in the area. As a consequence, given no reduction in landll activity or in refuse accessibility for gulls in landlls (Belant 1997), one can expect the region to sustain the future expansion of a species sometimes considered as superabundant (Vidal et al. 1998).
Acknowledgments We would like to thank Daniel Oro and an anonymous referee for invaluable comments on the rst version of the manuscript. We are most indebted to Carey Suehs and Ruth Menzies for their English editing of the manuscript. Many thanks are due to the following for their invaluable help in the eld: J. Legrand, the Staff of Port-Cros National Park (especially P. Vandenbrouck), A. Mante, D. Tatin, Y. Tranchant (Conservatoire` mes de Provence) and all volunteers. Funds Etudes des Ecosyste gional de Provence, and supports were provided by the Conseil Re te dAzur (contracts 99.00012.00 and 2002.16049), the Alpes, Co Port-Cros National Park (contracts 99.006.83400 PC and 00.006.83400 PC), and the ADEME (contract 02.40.038). This work is part of a scientic program directed by N. Sadoul (Station Biologique de la Tour du Valat).

Number Area (ha) Elevation (m) Isolation (m) GullDens82 na82 (ha) DK 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 1.1 95 89 2.5 28 21.5 18 90 0.5 2.3 15 6.5 16 2.5 1254 2.3 45 3 640 996 30 74 86 47 141 57 22 191 30 50 49 31 45 12 142 26 59 62 196 140 4,700 1,800 1,800 675 50 775 2,150 3,000 3,500 3,550 600 620 600 2,250 2,300 7,300 7,500 11,025 8,200 9,150 55.44 24.91 21.05 114.05 40.94 65.27 134.13 100.54 35.3 71.91 1.79 10.81 72.75 64.5 84.5 158.65 74.95 145.33 41.63 17.79 0.36 51.74 63.58 0.52 19.54 12.25 7.46 59.67 0.28 1.11 2.79 1.39 1.79 0.62 17.97 0.76 8.67 0.45 12.14 133.34 1.04 1.04 1.04 1.04 1.04 1.00 1.01 1.01 1.02 1.02 1.21 1.00 0.92 0.92 0.92 0.92 0.92 0.92 0.92 0.92

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