Ana Sanz-Aguilar

Kin recognition and inbreeding avoidance in wild birds: the first evidence for individual kin-related odour recognition

Identification of family members plays a primary role in the evolution of social behaviours such as nepotism, altruism and mate choice. The process is particularly important for philopatric species in which the encounter rate of kin-related conspecifics is high. Olfactory-based recognition of individual kin has been identified in most species, with the exception of birds; historically, birds were thought to have poor olfactory abilities, so the use of olfactory cues was ruled out a priori. Here, we show that European storm petrels, Hydrobates pelagicus, are able to distinguish kin from nonkin odours. Using special cotton swabs, like those used in forensic police procedures, we offered birds a binary choice in a Y-maze. Birds significantly preferred odours of unrelated individuals. Olfactory imprinting on a ‘family olfactory template’ or self-referent phenotype matching may be the mechanism underlying this effect. This choice behaviour may allow these highly philopatric birds to avoid inbreeding and select an appropriate mate. Our results suggest that sophisticated olfactory communication is relevant in birds, and leads to important behavioural traits such as philopatry.

The cost of reproduction and experience-dependent vital rates in a small petrel

Life history theory predicts that higher levels of reproductive investment entail higher reproductive costs especially among young and inexperienced individuals that might not optimize reproductive investment. Using a long-term individual and state-dependent capture-recapture data on Storm Petrels (Hydrobates pelagicus) we analyzed whether breeding experience and current breeding investment were associated with the expression of the cost of reproduction in terms of reduced survival and/or future breeding performance. We found a positive relationship between current breeding investment, breeding experience, and future survival and an improvement in breeding performance with individual experience independently of the previous breeding outcome. Our results suggest that the survival cost paid by first-time breeders and the positive correlation between reproduction and survival corresponds to selection against low quality birds unrelated to the breeding effort. Our work outlines the need to investigate the effect of multiple individual traits on different life history trade-offs simultaneously.

Modeling Trap-Awareness and Related Phenomena in Capture-Recapture Studies

Trap-awareness and related phenomena whereby successive capture events are not independent is a feature of the majority of capture-recapture studies. This phenomenon was up to now difficult to incorporate in open population models and most authors have chosen to neglect it although this may have damaging consequences. Focusing on the situation where animals exhibit a trap response at the occasion immediately following one where they have been trapped but revert to their original naïve state if they are missed once, we show that trap-dependence is more naturally viewed as a state transition and is amenable to the current models of capture-recapture. This approach has the potential to accommodate lasting or progressively waning trap effects.

To leave or not to leave: survival trade‐offs between different migratory strategies in the greater flamingo

1. The balance between costs and benefits of migration under different environmental, density-dependent and individual conditions may promote a broad range of migratory behaviours. We studied the factors influencing first-year migration and subsequent fidelity or dispersal among wintering areas, and the survival costs of different wintering behaviours in the greater flamingo (Phoenicopterus roseus). 2. We analysed by multievent capture-recapture modelling among-site dispersal/fidelity and site-dependent survival probabilities from 22 671 flamingos ringed in the Camargue (France) between 1977 and 2010 and resighted subsequently in their wintering grounds classified as France, Iberian Peninsula, Italy and North Africa. 3. We found that first- and second-year birds either resident or wintering at medium distances from their birth place, survived better than those wintering further afield. However, under severe winter conditions (extremely cold winter 1984-1985), individuals with the sedentary strategy suffered the highest levels of mortality. From the third winter onwards, the pattern of survival reversed: the long-distance wintering individuals (i.e. North Africa) survived better. 4. The proportion of first-year birds migrating for wintering was highly variable among cohorts and increased with favourable environmental conditions (wet years). After the first winter, birds showed high fidelity (>90%) to their previous wintering area and wintered preferably near their natal colony when they became adults (>2 years). 5. Survival estimates suggest that long-distance migration was costly for young and inexperienced individuals. Nonetheless, for adults, the most southern wintering areas seem to offer the most favourable local conditions for overwinter survival. 6. The higher availability of intermediate stopover sites during wet years may facilitate first-year migration. Then, once they have some wintering experience, flamingos appear to favour the known wintering grounds. As they grow older, dispersing towards the vicinity of the natal colony may provide higher breeding prospects for individuals wintering closer to this high-quality and saturated breeding ground, as predicted by the arrival-time hypothesis.

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 Corys 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.

Contrasting effects of climatic variability on the demography of a trans-equatorial migratory seabird

Large-scale seasonal climatic indices, such as the North Atlantic Oscillation (NAO) index or the Southern Oscillation Index (SOI), account for major variations in weather and climate around the world and may influence population dynamics in many organisms. However, assessing the extent of climate impacts on species and their life-history traits requires reliable quantitative statistical approaches. We used a new analytical tool in mark-recapture, the multi-event modelling, to simultaneously assess the influence of climatic variation on multiple demographic parameters (i.e. adult survival, transient probability, reproductive skipping and nest dispersal) at two Mediterranean colonies of the Corys shearwater Calonectris diomedea, a trans-equatorial migratory long-lived seabird. We also analysed the impact of climate in the breeding success at the two colonies. We found a clear temporal variation of survival for Corys shearwaters, strongly associated to the large-scale SOI especially in one of the colonies (up to 66% of variance explained). Atlantic hurricane season is modulated by the SOI and coincides with shearwater migration to their wintering areas, directly affecting survival probabilities. However, the SOI was a better predictor of survival probabilities than the frequency of hurricanes; thus, we cannot discard an indirect additive effect of SOI via food availability. Accordingly, the proportion of transients was also correlated with SOI values, indicating higher costs of first reproduction (resulting in either mortality or permanent dispersal) when bad environmental conditions occurred during winter before reproduction. Breeding success was also affected by climatic factors, the NAO explaining c. 41% of variance, probably as a result of its effect in the timing of peak abundance of squid and small pelagics, the main prey for shearwaters. No climatic effect was found either on reproductive skipping or on nest dispersal. Contrarily to what we expect for a long-lived organism, large-scale climatic indexes had a more pronounced effect on survival and transient probabilities than on less sensitive fitness parameters such reproductive skipping or nest dispersal probabilities. The potential increase in hurricane frequency because of global warming may interact with other global change agents (such as incidental bycatch and predation by alien species) nowadays impacting shearwaters, affecting future viability of populations.

Recapture processes and biological inference in monitoring burrow-nesting seabirds

Capture–mark–recapture methods are used widely for monitoring and diagnosis of bird populations as they permit robust estimates of population abundance and demographic parameters (e.g. survival) to be obtained from incomplete records of individual life histories. The statistical analysis of these data relies on the important assumption that individuals of the same local populations (i.e. colony) have the same parameters (the homogeneity assumption). We used data from six medium- to long-term monitoring schemes of local Mediterranean populations of the European Storm Petrel Hydrobates pelagicus to empirically show that the level of individual heterogeneity and the consequent bias in the parameter of interest depend on the recapture methodology, which has important consequences for the experimental design. We found that the recapture probability varied over time and among methodologies. The study design had a strong influence on the proportion of transients caught (i.e. individuals not recaptured after marking); however, the survival probability estimate for resident birds was fairly similar across the studies. The differences found in survival seem to depend on the biological variability between sites (e.g. predation pressure), and not on the recapture methods.

Links between fear of humans, stress and survival support a non-random distribution of birds among urban and rural habitats

Urban endocrine ecology aims to understand how organisms cope with new sources of stress and maintain allostatic load to thrive in an increasingly urbanized world. Recent research efforts have yielded controversial results based on short-term measures of stress, without exploring its fitness effects. We measured feather corticosterone (CORTf, reflecting the duration and amplitude of glucocorticoid secretion over several weeks) and subsequent annual survival in urban and rural burrowing owls. This species shows high individual consistency in fear of humans (i.e., flight initiation distance, FID), allowing us to hypothesize that individuals distribute among habitats according to their tolerance to human disturbance. FIDs were shorter in urban than in rural birds, but CORTf levels did not differ, nor were correlated to FIDs. Survival was twice as high in urban as in rural birds and links with CORTf varied between habitats: while a quadratic relationship supports stabilizing selection in urban birds, high predation rates may have masked CORTf-survival relationship in rural ones. These results evidence that urban life does not constitute an additional source of stress for urban individuals, as shown by their near identical CORTf values compared with rural conspecifics supporting the non-random distribution of individuals among habitats according to their behavioural phenotypes.

Multi‐event capture–recapture analysis reveals individual foraging specialization in a generalist species

Populations of species typically considered trophic generalists may include specialized individuals consistently feeding on certain resources. Optimal foraging theory states that individuals should feed on those resources most valuable to them. This, however, may vary according to individual differences in detecting or processing resources, different optimization criteria, and competitive abilities. White Storks (Ciconia ciconia) are trophic generalists at the population level. Their European population recovery has been attributed to increased wintering in southern Europe (rather than Africa) where they feed upon new anthropogenic food subsidies: predictable dumps and less predictable and more difficult to detect, but abundant, invasive Procambarus clarkii crayfishes in ricefields. We studied the foraging strategies of resident and wintering storks in southwestern Spain in ricefields and dumps, predicting that more experience in the study area (residents vs. immigrants, old vs. young) would increase rice...

Estimating recruitment and survival in partially monitored populations

Research funds were provided by the Spanish Ministries of Science, Economy and Competitiveness (refs. BOS2003-01960, CGL2006-04325/BOS, CGL2009-08298, CGL2013-42203-R, JCI-2011-09085)