Can attraction to and competition for high-quality habitats shape breeding propensity?

In many animal species, sexually mature individuals may skip breeding opportunities despite a likely negative impact on fitness. In spatio-temporally heterogeneous environments, habitat selection theory predicts that individuals select habitats where fitness prospects are maximized. Individuals are attracted to high-quality habitat patches where they compete for high-quality breeding sites. Since failures in contests to secure a site may prevent individuals from breeding, we hypothesized that attraction to and competition for high-quality habitats could shape breeding propensity. Under this hypothesis, we predicted the two following associations between breeding propensity and two key population features. (1) When mean habitat quality in the population increases in multiple patches such that availability of high-quality sites increases across the population, the resulting decrease in competition should positively affect breeding propensity. (2) When the number of individuals increases in the population, the resulting increase in competitors should negatively affect breeding propensity (negative density dependence). Using long-term data from kittiwakes Rissa tridactyla, we checked the prerequisite of prediction (1), that availability of high-quality sites is positively associated with current mean habitat quality in the population (represented by breeding success). We then applied integrated population modelling to quantify annual fluctuations in population mean breeding success, breeding propensity and number of individuals by breeding status (pre-breeders, breeders, skippers and immigrants), and tested our predictions. Our results showed that breeding propensity acts as an important driver of population growth. As expected, breeding propensity was positively associated with preceding mean habitat quality in the population, and negatively with the number of competitors. These relationships varied depending on breeding status, which likely reflects status dependence in competitive ability. These findings highlight the importance of competition for high-quality breeding sites in shaping breeding propensity. Thereby, we draw attention towards alternative and complementary explanations to more standard considerations regarding the energetic cost of reproduction, and point to possible side effects of habitat selection behaviours on individual life histories and population dynamics.

Breeding habitat selection across spatial scales: is grass always greener on the other side?

Habitat selection theory predicts that natural selection should favor mechanisms allowing individuals to choose habitats associated with the highest fitness prospects. However, identifying sources of information on habitat quality that individuals use to choose their breeding habitat has proved to be difficult. It has also proven difficult to identify dispersal costs that prevent individuals from joining the highest-quality sites. A synthesis that integrates dispersal costs and habitat selection mechanisms across space has remained elusive. Because costs of dispersal are generally distance-dependent, we suggest that a habitat selection strategy of sequential proximity search (SPS) can be favored by natural selection. This strategy requires that animals make decisions at multiple scales: whether to stay or leave the previous breeding site, depending on reproductive success; then, if dispersal is chosen, use information on neighborhood habitat quality to decide whether to stay in the neighborhood or leave, expanding the search area until the nearest suitable site is chosen. SPS minimizes distance-dependent dispersal costs while maximizing benefits of gaining a better habitat. We found evidence of breeding dispersal behavior consistent with this strategy in a kittiwake population stratified into a spatial hierarchy from colonies to nest sites. We used a mixed sequential regression model to study dispersal decisions, indexed by breeding dispersal movement, of 2,558 individuals over 32 yr. Scale-dependent dispersal propensities of kittiwakes varied according to breeding status, breeding experience, sex and individual identity. We suggest that distance-dependent dispersal costs result from strong competition among kittiwakes for nest sites. Individual decisions regarding dispersal (whether to leave or not, and where to go) depend on nesting habitat quality as well as the competitive ability required to keep territory ownership in a previous site, or to acquire a new site; this ability varies according to distance between sites and individual characteristics. Additional studies are needed to establish the generality of SPS in habitat selection.

Now you see him, now you don't: experience, not age, is related to reproduction in kittiwakes.

In long-lived species, individuals can skip reproduction. The proportion of breeders affects population growth rate and viability, there is a need to investigate the factors influencing intermittent breeding. The theory predicts that if lack of experience is an important constraint, breeding probabilities should increase with experience for individuals of the same age, whereas under the so-called restraint hypothesis, breeding probabilities should increase with age regardless of experience. However, because the probability of detecting individuals in the wild is generally less than 1, it is difficult to know exactly the number of previous breeding episodes (breeding experience). To cope with this issue, we developed a hidden process model to incorporate experience as a latent state possibly influencing the probability of breeding. Using a 22-year mark-recapture dataset involving 9970 individuals, we analysed simultaneously experience and age effects on breeding probabilities in the kittiwake (Rissa tridactyla). We did not detect an influence of age on adult breeding probabilities. We found that inexperienced birds breed less frequently than experienced birds. Our approach enables us to highlight the key role of experience on adults breeding probabilities and can be used for a wide range of organisms for which detection is less than 1.

Drivers of age-specific survival in a long-lived seabird: contributions of observed and hidden sources of heterogeneity.

1. We assessed the relative influence of variability in recruitment age, dynamic reproductive investment (time-specific reproductive states) and frailty (unobserved differences in survival abilities across individuals) on survival in the black-legged kittiwake. Furthermore, we examined whether observed variability in survival trajectories was best explained by immediate reproductive investment, cumulative investment, or both. 2. Individuals that delayed recruitment (≥ age 7) suffered a higher mortality risk than early recruits (age 3), especially later in life, suggesting that recruitment age may be an indicator of individual quality. Although recruitment age helped explain variation in survival, time-varying reproductive investment had a more substantial influence. 3. The dichotomy of attempting to breed or not explained variability in survival across life better than other parameterizations of reproductive states such as clutch size, brood size or breeding success. In the kittiwake, the sinequanon condition to initiate reproduction is to hold a nest site, which is considered a very competitive activity. This might explain why attempting to breed is the key level of investment that affects survival, independent of the outcome (failure or success). 4. Interestingly, the more individuals cumulate reproductive attempts over life, the lower their mortality risk, indicating that breeding experience may be a good indicator of parental quality as well. In contrast, attempting to breed at time t increased the risk of mortality between t and t + 1. We thus detected an immediate trade-off between attempting to breed and survival in this population; however, the earlier individuals recruited, and the more breeding experience they accumulated, the smaller the cost. 5. Lastly, unobserved heterogeneity across individuals improved model fit more (1·3 times) than fixed and dynamic sources of observed heterogeneity in reproductive investment, demonstrating that it is critical to account for both sources of individual heterogeneity when studying survival trajectories. Only after simultaneously accounting for both sources of heterogeneity were we able to detect the 'cost' of immediate reproductive investment on survival and the 'benefit' of cumulative breeding attempts (experience), a proxy to individual quality.

Consequences of recruitment decisions and heterogeneity on age-specific breeding success in a long-lived seabird.

An individual's age at first reproduction and investment in successive reproductive attempts are involved in mechanisms that can impede somatic repair, resulting in a decline in reproductive abilities with age (reproductive senescence). We used long-term data from the Black-legged Kittiwake, a long-lived seabird, to address the relationship between recruitment age, age-specific breeding success (BS), and reproductive senescence, while accounting for breeding experience and temporal variation in BS. We first detected late-life improvement in BS across all recruitment groups, which we recognized as "within-generation selection" or the selective disappearance of "frail" phenotypes. When such heterogeneity was accurately accounted for, we showed that all individuals suffered reproductive senescence. We first highlighted how different combinations of pre- and post-recruitment experience across recruitment groups resulted in maximal BS at intermediate ages. BS increased in early recruits as they gained post-recruitment experience, whereas late recruits gained pre-recruitment experience that led to high BS at recruitment. Only individuals recruiting at intermediate ages balanced their pre- and post-recruitment experience. Consistent with the "cumulative reproductive cost hypothesis," we also observed a faster decline in BS in early recruits at advanced ages, whereas individuals delaying recruitment experienced the slowest decline in BS with age. Early recruits, however, reached the highest levels of BS at intermediate ages, sensus stricto (10-13 years old), whereas individuals delaying recruitment experienced the lowest at similar ages. These divergent trajectories may reflect a "delayed trade-off" balancing a maximization of midlife BS against reproductive senescence at advanced ages. Additionally, annual variation in BS had a greater effect on individuals early in life, suggesting that experienced individuals were able to buffer out the effects of temporal variation on BS, which can ultimately improve fitness in stochastic environments. Our findings stress that (1) both observed and unobserved heterogeneity are important in detecting within-individual senescence, and (2) short-term trade-offs may be rare in long-lived species; thus, cumulated reproductive costs should be invoked as an alternative mechanism underlying reproductive senescence.

Individual covariation in life-history traits: seeing the trees despite the forest.

We investigated the influence of age on survival and breeding rates in a long-lived species Rissa tridactyla using models with individual random effects permitting variation and covariation in fitness components among individuals. Differences in survival or breeding probabilities among individuals are substantial, and there was positive covariation between survival and breeding probability; birds that were more likely to survive were also more likely to breed, given that they survived. The pattern of age-related variation in these rates detected at the individual level differed from that observed at the population level. Our results provided confirmation of what has been suggested by other investigators: within-cohort phenotypic selection can mask senescence. Although this phenomenon has been extensively studied in humans and captive animals, conclusive evidence of the discrepancy between population-level and individual-level patterns of age-related variation in life-history traits is extremely rare in wild animal populations. Evolutionary studies of the influence of age on life-history traits should use approaches differentiating population level from the genuine influence of age: only the latter is relevant to theories of life-history evolution. The development of models permitting access to individual variation in fitness is a promising advance for the study of senescence and evolutionary processes.