Life span, growth, senescence and island syndrome: Accounting for imperfect detection and continuous growth.

Small vertebrates on islands are expected to attain a larger body size, and a greater survival than their mainland counterparts. Comparative studies have questioned whether lizards exhibit this set of adaptations, referred to as the 'island syndrome'. We collected data on 730 individuals the endemic Lilford's lizard Podarcis lilfordi throughout a 10-year period on a small island of the Balearic archipelago (Spain). We coupled a growth function with a capture-mark-recapture model to simultaneously estimate size- and sex-dependent growth rate and survival. To put our results into a wider context, we conducted a systematic review of growth, life span and age at maturity in different Podarcis species comparing insular and mainland populations. We found a low average growth coefficient (0.56 and 0.41 year-1 for males and females to reach an asymptotic size of 72.3 and 65.6 mm respectively), a high annual survival probability of 0.81 and 0.79 in males and females, and a large variability between individuals in growth parameters. Survival probability decreased with body size in both sexes, indicating a senescence pattern typical of long-lived species or in populations with a low extrinsic mortality. Assuming a constant survival after sexual maturity, at about 2 years old, the average life span was 6.18 years in males and 8.99 in females. The oldest animal was a male last captured at an estimated age of ≥13 years and still alive at the end of the study. Our results agree with the predictions of the 'island syndrome' for survival, life span and growth parameters. A comparative analysis of these values across 29 populations of 16 different species of Podarcis indicated that insular lizards grow slower and live longer than their mainland counterparts. However, our data differed from other island populations of the same species, suggesting that island-specific characteristics play an additional role to isolation. Within this study we developed an analytical approach to study the body size-dependent survival of small reptiles. We discuss its applicability to contrast hypotheses on senescence in different sexes of this species, and provide the code used to integrate the growth and capture-mark-recapture models.

Active breeding seabirds prospect alternative breeding colonies.

Compared to other animal movements, prospecting by adult individuals for a future breeding site is commonly overlooked. Prospecting influences the decision of where to breed and has consequences on fitness and lifetime reproductive success. By analysing movements of 31 satellite- and GPS-tracked gull and tern populations belonging to 14 species in Europe and North America, we examined the occurrence and factors explaining prospecting by actively breeding birds. Prospecting in active breeders occurred in 85.7% of studied species, across 61.3% of sampled populations. Prospecting was more common in populations with frequent inter-annual changes of breeding sites and among females. These results contradict theoretical models which predict that prospecting is expected to evolve in relatively predictable and stable environments. More long-term tracking studies are needed to identify factors affecting patterns of prospecting in different environments and understand the consequences of prospecting on fitness at the individual and population level.

Differential adult survival at close seabird colonies: The importance of spatial foraging segregation and bycatch risk during the breeding season.

Marine megafauna, including seabirds, are critically affected by fisheries bycatch. However, bycatch risk may differ on temporal and spatial scales due to the uneven distribution and effort of fleets operating different fishing gear, and to focal species distribution and foraging behavior. Scopoli's shearwater Calonectris diomedea is a long-lived seabird that experiences high bycatch rates in longline fisheries and strong population-level impacts due to this type of anthropogenic mortality. Analyzing a long-term dataset on individual monitoring, we compared adult survival (by means of multi-event capture-recapture models) among three close predator-free Mediterranean colonies of the species. Unexpectedly for a long-lived organism, adult survival varied among colonies. We explored potential causes of this differential survival by (1) measuring egg volume as a proxy of food availability and parental condition; (2) building a specific longline bycatch risk map for the species; and (3) assessing the distribution patterns of breeding birds from the three study colonies via GPS tracking. Egg volume was very similar between colonies over time, suggesting that environmental variability related to habitat foraging suitability was not the main cause of differential survival. On the other hand, differences in foraging movements among individuals from the three colonies expose them to differential mortality risk, which likely influenced the observed differences in adult survival. The overlap of information obtained by the generation of specific bycatch risk maps, the quantification of population demographic parameters, and the foraging spatial analysis should inform managers about differential sensitivity to the anthropogenic impact at mesoscale level and guide decisions depending on the spatial configuration of local populations. The approach would apply and should be considered in any species where foraging distribution is colony-specific and mortality risk varies spatially.

Varying demographic impacts of different fisheries on three Mediterranean seabird species.

Fisheries have an enormous economic importance, but reconciling their socio-economic features with the conservation and sustainability of marine ecosystems presents major challenges. Bycatch mortality from fisheries is clearly among the most serious global threats for marine ecosystems, affecting a wide range of top predators. Recent estimates report ca. 200,000 seabirds killed annually by bycatch in European waters. However, there is an urgent need to rigorously estimate actual mortality rates and quantify effects of bycatch on populations. The Mediterranean Sea is one of the most impacted regions. Here, we estimate for the first time both bycatch mortality rates and their population-level effects on three endemic and vulnerable Mediterranean taxa: Scopoli's shearwater, Mediterranean shag, and Audouin's gull, that die in different types of fishing gears: longlines, gillnets and sport trolling, respectively. We use multi-event capture-recapture modelling to estimate crucial demographic parameters, including the probabilities of dying in different fishing gears. We then build stochastic demography models to forecast the viability of the populations under different management scenarios. Longline bycatch was particularly severe for adults of Scopoli's shearwaters and Audouin's gulls (ca. 28% and 23% of total mortality, respectively) and also for immature gulls (ca. 90% of mortality). Gillnets had a lower impact, but were still responsible for ca. 9% of juvenile mortality on shags, whereas sport trolling only slightly influenced total mortality in gulls. Bycatch mortality has high population-level impacts in all three species, with shearwaters having the highest extinction risk under current mortality rates. Different life-history traits and compensatory demographic mechanisms between the three species are probably influencing the different bycatch impact: for shearwaters, urgent conservation actions are required to ensure the viability of their populations. Results will be very useful for guiding future seabird conservation policies and moving towards an ecosystem-based approach to sustainable fisheries management.

Climate-driven vital rates do not always mean climate-driven population.

Current climatic changes have increased the need to forecast population responses to climate variability. A common approach to address this question is through models that project current population state using the functional relationship between demographic rates and climatic variables. We argue that this approach can lead to erroneous conclusions when interpopulation dispersal is not considered. We found that immigration can release the population from climate-driven trajectories even when local vital rates are climate dependent. We illustrated this using individual-based data on a trans-equatorial migratory seabird, the Scopoli's shearwater Calonectris diomedea, in which the variation of vital rates has been associated with large-scale climatic indices. We compared the population annual growth rate λi , estimated using local climate-driven parameters with ρi , a population growth rate directly estimated from individual information and that accounts for immigration. While λi varied as a function of climatic variables, reflecting the climate-dependent parameters, ρi did not, indicating that dispersal decouples the relationship between population growth and climate variables from that between climatic variables and vital rates. Our results suggest caution when assessing demographic effects of climatic variability especially in open populations for very mobile organisms such as fish, marine mammals, bats, or birds. When a population model cannot be validated or it is not detailed enough, ignoring immigration might lead to misleading climate-driven projections.

Population control of an overabundant species achieved through consecutive anthropogenic perturbations.

The control of overabundant vertebrates is often problematic. Much work has focused on population-level responses and overabundance due to anthropogenic subsidies. However, far less work has been directed at investigating responses following the removal of subsidies. We investigate the consequences of two consecutive perturbations, the closure of a landfill and an inadvertent poisoning event, on the trophic ecology (δ13C, δ15N, and δ34S), survival, and population size of an overabundant generalist seabird species, the Yellow-legged Gull (Larus michahellis). We expected that the landfill closure would cause a strong dietary shift and the inadvertent poisoning a decrease in gull population size. As a long-lived species, we also anticipated adult survival to be buffered against the decrease in food availability but not against the inadvertent poisoning event. Stable isotope analysis confirmed the dietary shift towards marine resources after the disappearance of the landfill. Although the survival model was inconclusive, it did suggest that the perturbations had a negative effect on survival, which was followed by a recovery back to average values. Food limitation likely triggered dispersal to other populations, while poisoning may have increased mortality; these two processes were likely responsible for the large fall in population size that occurred after the two consecutive perturbations. Life-history theory suggests that perturbations may encourage species to halt existing breeding investment in order to ensure future survival. However, under strong perturbation pulses the resilience threshold might be surpassed and changes in population density can arise. Consecutive perturbations may effectively manage overabundant species.

Population genetics and phylogeographic history of the insular lizard Podarcis lilfordi (Gunther, 1874) from the Balearic Islands based on genome-wide polymorphic data.

Islands provide a great system to explore the processes that maintain genetic diversity and promote local adaptation. We explored the genomic diversity of the Balearic lizard Podarcis lilfordi, an endemic species characterized by numerous small insular populations with large phenotypic diversity. Using the newly available genome for this species, we characterized more than 300,000 SNPs, merging genotyping-by-sequencing (GBS) data with previously published restriction site-associated DNA sequencing (RAD-Seq) data, providing a dataset of 16 island populations (191 individuals) across the range of species distribution (Menorca, Mallorca, and Cabrera). Results indicate that each islet hosts a well-differentiated population (F ST = 0.247 ± 0.09), with no recent immigration/translocation events. Contrary to expectations, most populations harbor a considerable genetic diversity (mean nucleotide diversity, P i = 0.144 ± 0.021), characterized by overall low inbreeding values (F IS < 0.1). While the genetic diversity significantly decreased with decreasing islet surface, maintenance of substantial genetic diversity even in tiny islets suggests variable selection or other mechanisms that buffer genetic drift. Maximum-likelihood tree based on concatenated SNP data confirmed the existence of the two major independent lineages of Menorca and Mallorca/Cabrera. Multiple lines of evidence, including admixture and root testing, robustly placed the origin of the species in the Mallorca Island, rather than in Menorca. Outlier analysis mainly retrieved a strong signature of genome differentiation between the two major archipelagos, especially in the sexual chromosome Z. A set of proteins were target of multiple outliers and primarily associated with binding and catalytic activity, providing interesting candidates for future selection studies. This study provides the framework to explore crucial aspects of the genetic basis of phenotypic divergence and insular adaptation.

Insular holobionts: persistence and seasonal plasticity of the Balearic wall lizard (Podarcis lilfordi) gut microbiota.

Background: Integrative studies of animals and associated microbial assemblages (i.e., the holobiont) are rapidly changing our perspectives on organismal ecology and evolution. Insular vertebrates provide ideal natural systems to understand patterns of host-gut microbiota coevolution, the resilience and plasticity these microbial communities over temporal and spatial scales, and ultimately their role in the host ecological adaptation. Methods: Here we used the endemic Balearic wall lizard Podarcis lilfordi to dissect the drivers of the microbial diversity within and across host allopatric populations/islets. By focusing on three extensively studied populations/islets of Mallorca (Spain) and fecal sampling from individually identified lizards along two years (both in spring and autumn), we sorted out the effect of islet, sex, life stage, year and season on the microbiota composition. We further related microbiota diversity to host genetics, trophic ecology and expected annual metabolic changes. Results: All the three populations showed a remarkable conservation of the major microbial taxonomic profile, while carrying their unique microbial signature at finer level of taxonomic resolution (Amplicon Sequence Variants (ASVs)). Microbiota distances across populations were compatible with both host genetics (based on microsatellites) and trophic niche distances (based on stable isotopes and fecal content). Within populations, a large proportion of ASVs (30-50%) were recurrently found along the four sampling dates. The microbial diversity was strongly marked by seasonality, with no sex effect and a marginal life stage and annual effect. The microbiota showed seasonal fluctuations along the two sampled years, primarily due to changes in the relative abundances of fermentative bacteria (mostly families Lachnospiraceae and Ruminococcaceae), without any major compositional turnover. Conclusions: These results support a large resilience of the major compositional aspects of the P. lilfordi gut microbiota over the short-term evolutionary divergence of their host allopatric populations (<10,000 years), but also indicate an undergoing process of parallel diversification of the both host and associated gut microbes. Predictable seasonal dynamics in microbiota diversity suggests a role of microbiota plasticity in the lizards' metabolic adaptation to their resource-constrained insular environments. Overall, our study supports the need for longitudinal and integrative studies of host and associated microbes in natural systems.

Interspecific synchrony on breeding performance and the role of anthropogenic food subsidies.

Synchrony can have important consequences for long-term metapopulations persistence, community dynamics and ecosystems functioning. While the causes and consequences of intra-specific synchrony on population size and demographic rates have received considerable attention only a few factors that may affect inter-specific synchrony have been described. We formulate the hypothesis that food subsidies can buffer the influence of environmental stochasticity on community dynamics, disrupting and masking originally synchronized systems. To illustrate this hypothesis, we assessed the consequences of European policies implementation affecting subsidy availability on the temporal synchrony of egg volume as a proxy of breeding investment in two sympatric marine top predators with differential subsidy use. We show how 7-year synchrony appears on egg volume fluctuations after subsidy cessation suggesting that food subsidies could disrupt interspecific synchrony. Moreover, cross correlation increased after subsidy cessation and environmental buffering seems to act during synchronization period. We emphasize that subsidies dynamics and waste management provide novel insights on the emergence of synchrony in natural populations.

It's not all abundance: Detectability and accessibility of food also explain breeding investment in long-lived marine animals.

Large-scale climatic indices are extensively used as predictors of ecological processes, but the mechanisms and the spatio-temporal scales at which climatic indices influence these processes are often speculative. Here, we use long-term data to evaluate how a measure of individual breeding investment (the egg volume) of three long-lived and long-distance-migrating seabirds is influenced by i) a large-scale climatic index (the North Atlantic Oscillation) and ii) local-scale variables (food abundance, foraging conditions, and competition). Winter values of the North Atlantic Oscillation did not correlate with local-scale variables measured in spring, but surprisingly, both had a high predictive power of the temporal variability of the egg volume in the three study species, even though they have different life-history strategies. The importance of the winter North Atlantic Oscillation suggests carry-over effects of winter conditions on subsequent breeding investment. Interestingly, the most important local-scale variables measured in spring were associated with food detectability (foraging conditions) and the factors influencing its accessibility (foraging conditions and competition by density-dependence). Large-scale climatic indices may work better as predictors of foraging conditions when organisms perform long distance migrations, while local-scale variables are more appropriate when foraging areas are more restricted (e.g. during the breeding season). Contrary to what is commonly assumed, food abundance does not directly translate into food intake and its detectability and accessibility should be considered in the study of food-related ecological processes.

Studying the reproductive skipping behavior in long-lived birds by adding nest inspection to individual-based data.

The frequency at which individuals breed is an important parameter in population, as well as in evolutionary, studies. However, when nonbreeding individuals are absent from the study area, the reproductive skipping is usually confounded with a recapture failure and cannot be estimated directly. Yet, there are situations in which external information may help to estimate reproductive skipping. Such a situation is found with nest-tenacious birds: the fact that an individual is not encountered in its previous nest is a good indication that it must be skipping reproduction. We illustrate here a general probabilistic framework in which we merged the classical individual capture-recapture information with nest-based information to obtain the simultaneous estimate of recapture, survival, reproductive skipping, and within-colony breeding dispersal probabilities using multi-event models. We applied this approach to Cory's Shearwater (Calonectris diomedea), a long-lived burrow-nesting seabird. By comparing results with those obtained from the analysis of the capture-recapture information alone, we showed that the model separates successfully the probabilities of recapture from those of temporal emigration. We found that the probabilities of future reproduction and breeding-site fidelity were lower for individuals temporarily absent from the colony, suggesting a lower intrinsic quality of intermittent breeders. The new probabilistic framework presented here allowed us to refine the estimates of demographic parameters by simply adding nest-based data, a type of information usually collected in the field but never included in the analysis of individual-based data. Our approach also provides a new and flexible way to test hypotheses on temporal emigration and breeding dispersal in longitudinal data.

Global political responsibility for the conservation of albatrosses and large petrels.

Migratory marine species cross political borders and enter the high seas, where the lack of an effective global management framework for biodiversity leaves them vulnerable to threats. Here, we combine 10,108 tracks from 5775 individual birds at 87 sites with data on breeding population sizes to estimate the relative year-round importance of national jurisdictions and high seas areas for 39 species of albatrosses and large petrels. Populations from every country made extensive use of the high seas, indicating the stake each country has in the management of biodiversity in international waters. We quantified the links among national populations of these threatened seabirds and the regional fisheries management organizations (RFMOs) which regulate fishing in the high seas. This work makes explicit the relative responsibilities that each country and RFMO has for the management of shared biodiversity, providing invaluable information for the conservation and management of migratory species in the marine realm.

Contrasting size-dependent life history strategies of an insular lizard.

In many species with continuous growth, body size is an important driver of life-history tactics and its relative importance is thought to reflect the spatio-temporal variability of selective pressures. We developed a deterministic size-dependent integral projection model for 3 insular neighboring lizard populations with contrasting adult body sizes to investigate how size-related selective pressures can influence lizard life-history tactics. For each population, we broke down differences in population growth rates into contributions from size-dependent body growth, survival, and fecundity. A life table response experiment (LTRE) was used to compare the population dynamics of the 3 populations and quantify the contributions of intrinsic demographic coefficients of each population to the population growth rate (λ). Perturbation analyses revealed that the largest adults contributed the most to the population growth rate, but this was not true in the population with the smallest adults and size-independent fertility. Although we were not able to identify a single factor responsible for this difference, the combination of the demographic model on a continuous trait coupled with an LTRE analysis revealed how individuals from sister populations of the same species follow different life strategies and showed different compensatory mechanisms among survival, individual body growth, and fertility. Our results indicate that body size can play a contrasting role even in closely-related and closely-spaced populations.

Diet composition of the lizard Podarcis lilfordi (Lacertidae) on 2 small islands: an individual-resource network approach.

Despite it is widely accepted that intrapopulation variation is fundamental to ecological and evolutionary processes, this level of information has only recently been included into network analysis of species/population interactions. When done, it has revealed non-random patterns in the distribution of trophic resources. Nestedness in resource use among individuals is the most recurrent observed pattern, often accompanied by an absence of modularity, but no previous studies examine bipartite modularity. We use network analysis to describe the diet composition of the Balearic endemic lizard Podarcis lilfordi in 2 islets at population and individual levels, based on the occurrence of food items in fecal samples. Our objectives are to 1) compare niche structure at both levels, 2) characterize niche partition using nestedness and modularity, and 3) assess how size, sex, season, and spatial location influence niche structure. At population-level niche width was wide, but narrow at the level of the individual. Both islet networks were nested, indicating similar ranking of the food preferences among individuals, but also modular, which was partially explained by seasonality. Sex and body size did not notably affect diet composition. Large niche overlap and therefore possibly relaxed competition were observed among females in one of the islets and during spring on both islets. Likewise, higher modularity in autumn suggests that higher competition could lead to specialization in both populations, because resources are usually scarce in this season. The absence of spatial location influence on niche might respond to fine-grained spatio-temporally distribution of food resources. Behavioral traits, not included in this study, could also influence resource partitioning.

Infestation of small seabirds by Ornithodoros maritimus ticks: Effects on chick body condition, reproduction and associated infectious agents.

Ticks can negatively affect their host by direct effects as blood feeding causing anaemia or discomfort, or by pathogen transmission. Consequently, ticks can have an important role in the population dynamics of their hosts. However, specific studies on the demographic effects of tick infestation on seabirds are still scarce. Seabird ticks have also the potential to be responsible for the circulation of little known tick-borne agents, which could have implications for non-seabird species. Here, we report the results of investigations on potential associations between soft tick Ornithodoros maritimus load and reproductive parameters of storm petrels Hydrobates pelagicus breeding in a large colony in a cave of Espartar Island, in the Balearic archipelago. We also investigated by molecular analyses the potential viral and bacterial pathogens associated with O. maritimus ticks present at the colony. Lower nestling survival was recorded in the most infested area, deep in the cave, compared to the area near the entrance. The parasite load was negatively associated with the body condition of the nestlings. One pool of ticks tested positive for West Nile virus and 4 pools tested positive for a Borrelia species which was determined by targeted nested PCR to have a 99% sequence identity with B. turicatae, a relapsing fever Borrelia. Overall, these results show that further investigations are needed to better understand the ecology and epidemiology of the interactions between ticks, pathogens and Procellariiform species.

Foraging segregation between two closely related shearwaters breeding in sympatry.

Trophic segregation has been proposed as a major mechanism explaining the coexistence of closely related animal taxa. However, how such segregation varies throughout the annual cycle is poorly understood. Here, we examined the feeding ecology of the two subspecies of Cory's shearwater, Calonectris diomedea diomedea and Calonectris diomedea borealis, breeding in sympatry in a Mediterranean colony. To study trophic segregation at different stages, we combined the analysis of isotope values (delta(15)N, delta(13)C) in blood obtained during incubation and in feathers moulted during chick-rearing and wintering periods with satellite-tracking data during the chick-rearing period. Satellite-tracking and stable isotope data of the first primary feather revealed that C. d. borealis foraged mainly in the Atlantic whereas C. d. diomedea foraged exclusively in the Mediterranean. This spatial segregation could reflect the foraging behaviour of the C. d. borealis individuals before they arrived at the Mediterranean colony. Alternatively, greater wing loading of C. d. borealis individuals may confer the ability to fly across the strong winds occurring at the at the Gibraltar strait. Isotope values of the eighth secondary feather also support segregation in wintering areas between the two forms: C. d. diomedea wintered mainly in association with the Canary current, whereas C. d. borealis wintered in the South African coast. Overall, our results show that spatial segregation in foraging areas can display substantial variation throughout the annual cycle and is probably a major mechanism facilitating coexistence between closely related taxa.

Population structure and dispersal patterns within and between Atlantic and Mediterranean populations of a large-range pelagic seabird.

Dispersal is critically linked to the demographic and evolutionary trajectories of populations, but in most seabird species it may be difficult to estimate. Using molecular tools, we explored population structure and the spatial dispersal pattern of a highly pelagic but philopatric seabird, the Cory's shearwater Calonectris diomedea. Microsatellite fragments were analysed from samples collected across almost the entire breeding range of the species. To help disentangle the taxonomic status of the two subspecies described, the Atlantic form C. d. borealis and the Mediterranean form C. d. diomedea, we analysed genetic divergence between subspecies and quantified both historical and recent migration rates between the Mediterranean and Atlantic basins. We also searched for evidence of isolation by distance (IBD) and addressed spatial patterns of gene flow. We found a low genetic structure in the Mediterranean basin. Conversely, strong genetic differentiation appeared in the Atlantic basin. Even if the species was mostly philopatric (97%), results suggest recent dispersal between basins, especially from the Atlantic to the Mediterranean (aprox. 10% of migrants/generation across the last two generations). Long-term gene flow analyses also suggested an historical exchange between basins (about 70 breeders/generation). Spatial analysis of genetic variation indicates that distance is not the main factor in shaping genetic structure in this species. Given our results we recommend gathering more data before concluded whether these taxa should be treated as two species or subspecies.

Buying years to extinction: is compensatory mitigation for marine bycatch a sufficient conservation measure for long-lived seabirds?

Along the lines of the 'polluter pays principle', it has recently been proposed that the local long-line fishing industry should fund eradication of terrestrial predators at seabird breeding colonies, as a compensatory measure for the bycatch caused by the fishing activity. The measure is economically sound, but a quantitative and reliable test of its biological efficacy has never been conducted. Here, we investigated the demographic consequences of predator eradication for Cory's shearwater Calonectris diomedea, breeding in the Mediterranean, using a population model that integrates demographic rates estimated from individual life-history information with experimental measures of predation and habitat structure. We found that similar values of population growth rate can be obtained by different combinations of habitat characteristics, predator abundance and adult mortality, which explains the persistence of shearwater colonies in islands with introduced predators. Even so, given the empirically obtained values of survival, all combinations of predator abundance and habitat characteristics projected a decline in shearwater numbers. Perturbation analyses indicated that the value and the sensitivity of shearwater population growth rates were affected by all covariates considered and their interactions. A decrease in rat abundance delivered only a small increase in the population growth rate, whereas a change in adult survival (a parameter independent of rat abundance) had the strongest impact on population dynamics. When adult survival is low, rat eradication would allow us to "buy" years before extinction but does not reverse the process. Rat eradication can therefore be seen as an emergency measure if threats on adult survival are eliminated in the medium-term period. For species with low fecundity and long life expectancy, our results suggest that rat control campaigns are not a sufficient, self-standing measure to compensate the biological toll of long-line fisheries.