Temporal correlations among demographic parameters are ubiquitous but highly variable across species.

Temporal correlations among demographic parameters can strongly influence population dynamics. Our empirical knowledge, however, is very limited regarding the direction and the magnitude of these correlations and how they vary among demographic parameters and species' life histories. Here, we use long-term demographic data from 15 bird and mammal species with contrasting pace of life to quantify correlation patterns among five key demographic parameters: juvenile and adult survival, reproductive probability, reproductive success and productivity. Correlations among demographic parameters were ubiquitous, more frequently positive than negative, but strongly differed across species. Correlations did not markedly change along the slow-fast continuum of life histories, suggesting that they were more strongly driven by ecological than evolutionary factors. As positive temporal demographic correlations decrease the mean of the long-run population growth rate, the common practice of ignoring temporal correlations in population models could lead to the underestimation of extinction risks in most species.

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.

Uncovering ecological state dynamics with hidden Markov models.

Ecological systems can often be characterised by changes among a finite set of underlying states pertaining to individuals, populations, communities or entire ecosystems through time. Owing to the inherent difficulty of empirical field studies, ecological state dynamics operating at any level of this hierarchy can often be unobservable or 'hidden'. Ecologists must therefore often contend with incomplete or indirect observations that are somehow related to these underlying processes. By formally disentangling state and observation processes based on simple yet powerful mathematical properties that can be used to describe many ecological phenomena, hidden Markov models (HMMs) can facilitate inferences about complex system state dynamics that might otherwise be intractable. However, HMMs have only recently begun to gain traction within the broader ecological community. We provide a gentle introduction to HMMs, establish some common terminology, review the immense scope of HMMs for applied ecological research and provide a tutorial on implementation and interpretation. By illustrating how practitioners can use a simple conceptual template to customise HMMs for their specific systems of interest, revealing methodological links between existing applications, and highlighting some practical considerations and limitations of these approaches, our goal is to help establish HMMs as a fundamental inferential tool for ecologists.

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.

Wolf in sheep's clothing: Model misspecification undermines tests of the neutral theory for life histories.

Understanding the processes behind change in reproductive state along life-history trajectories is a salient research program in evolutionary ecology. Two processes, state dependence and heterogeneity, can drive the dynamics of change among states. Both processes can operate simultaneously, begging the difficult question of how to tease them apart in practice. The Neutral Theory for Life Histories (NTLH) holds that the bulk of variations in life-history trajectories is due to state dependence and is hence neutral: Once previous (breeding) state is taken into account, variations are mostly random. Lifetime reproductive success (LRS), the number of descendants produced over an individual's reproductive life span, has been used to infer support for NTLH in natura. Support stemmed from accurate prediction of the population-level distribution of LRS with parameters estimated from a state dependence model. We show with Monte Carlo simulations that the current reliance of NTLH on LRS prediction in a null hypothesis framework easily leads to selecting a misspecified model, biased estimates and flawed inferences. Support for the NTLH can be spurious because of a systematic positive bias in estimated state dependence when heterogeneity is present in the data but ignored in the analysis. This bias can lead to spurious positive covariance between fitness components when there is in fact an underlying trade-off. Furthermore, neutrality implied by NTLH needs a clarification because of a probable disjunction between its common understanding by evolutionary ecologists and its translation into statistical models of life-history trajectories. Irrespective of what neutrality entails, testing hypotheses about the dynamics of change among states in life histories requires a multimodel framework because state dependence and heterogeneity can easily be mistaken for each other.

The Conundrum of Heterogeneities in Life History Studies.

What causes interindividual variation in fitness? Evidence of heritability of latent individual fitness traits has resparked a debate about the causes of variation in life histories in populations: neutralism versus empirical adaptationism. This debate about the processes underlying observed variation pits neutral stochastic demographic processes against evolutionarily relevant differences among individual fitness traits. Advancing this debate requires careful consideration of differences among inference approaches used by proponents of each hypothesis. Here we draw parallels between several disciplines focusing on processes generating variation in individuals' life-course, and we contrast methodologies to disentangle these processes. We draw on other disciplines to clarify terminology, risks of flawed inference, and expand the panel of hypotheses and formalizations of processes generating variation in life histories.

Archiving Primary Data: Solutions for Long-Term Studies.

The recent trend for journals to require open access to primary data included in publications has been embraced by many biologists, but has caused apprehension amongst researchers engaged in long-term ecological and evolutionary studies. A worldwide survey of 73 principal investigators (Pls) with long-term studies revealed positive attitudes towards sharing data with the agreement or involvement of the PI, and 93% of PIs have historically shared data. Only 8% were in favor of uncontrolled, open access to primary data while 63% expressed serious concern. We present here their viewpoint on an issue that can have non-trivial scientific consequences. We discuss potential costs of public data archiving and provide possible solutions to meet the needs of journals and researchers.

The evolutionary significance of latent reproductive rate in a long-lived vertebrate.

Chambert, Rotella & Garrott () used long-term data to assess the evolutionary significance of individual latent reproductive rate in female Weddell seals. Latent reproductive rates capture the differences among individuals in terms of their propensity to breed; they are conceptual and mathematical constructs. Neither recruitment probability nor age of first breeding of daughters was related to the mother's latent reproductive rate, but there was evidence of a weak positive relationship between the latent reproductive rates of mothers and daughters, suggesting some degree of heritability in this trait. Females with a high latent reproductive rate were expected to produce 2·0 times as many recruited females and 2·1 times as many grandchildren as females with a low reproductive rate. There was substantial stochastic variation in the number of offspring and grandchildren produced, but the inter-individual variability in female latent reproductive rate may have important fitness consequences.

Variation in size and growth of the great scallop Pecten maximus along a latitudinal gradient.

Understanding the relationship between growth and temperature will aid in the evaluation of thermal stress and threats to ectotherms in the context of anticipated climate changes. Most Pecten maximus scallops living at high latitudes in the northern hemisphere have a larger maximum body size than individuals further south, a common pattern among many ectotherms. We investigated differences in daily shell growth among scallop populations along the Northeast Atlantic coast from Spain to Norway. This study design allowed us to address precisely whether the asymptotic size observed along a latitudinal gradient, mainly defined by a temperature gradient, results from differences in annual or daily growth rates, or a difference in the length of the growing season. We found that low annual growth rates in northern populations are not due to low daily growth values, but to the smaller number of days available each year to achieve growth compared to the south. We documented a decrease in the annual number of growth days with age regardless of latitude. However, despite initially lower annual growth performances in terms of growing season length and growth rate, differences in asymptotic size as a function of latitude resulted from persistent annual growth performances in the north and sharp declines in the south. Our measurements of daily growth rates throughout life in a long-lived ectothermic species provide new insight into spatio-temporal variations in growth dynamics and growing season length that cannot be accounted for by classical growth models that only address asymptotic size and annual growth rate.

Assessing hypotheses about nesting site occupancy dynamics.

Hypotheses about habitat selection developed in the evolutionary ecology framework assume that individuals, under some conditions, select breeding habitat based on expected fitness in different habitat. The relationship between habitat quality and fitness may be reflected by breeding success of individuals, which may in turn be used to assess habitat quality. Habitat quality may also be assessed via local density: if high-quality sites are preferentially used, high density may reflect high-quality habitat. Here we assessed whether site occupancy dynamics vary with site surrogates for habitat quality. We modeled nest site use probability in a seabird subcolony (the Black-legged Kittiwake, Rissa tridactyla) over a 20-year period. We estimated site persistence (an occupied site remains occupied from time t to t+1) and colonization through two subprocesses: first colonization (site creation at the timescale of the study) and recolonization (a site is colonized again after being deserted). Our model explicitly incorporated site-specific and neighboring breeding success and conspecific density in the neighborhood. Our results provided evidence that reproductively "successful" sites have a higher persistence probability than "unsuccessful" ones. Analyses of site fidelity in marked birds and of survival probability showed that high site persistence predominantly reflects site fidelity, not immediate colonization by new owners after emigration or death of previous owners. There is a negative quadratic relationship between local density and persistence probability. First colonization probability decreases with density, whereas recolonization probability is constant. This highlights the importance of distinguishing initial colonization and recolonization to understand site occupancy. All dynamics varied positively with neighboring breeding success. We found evidence of a positive interaction between site-specific and neighboring breeding success. We addressed local population dynamics using a site occupancy approach integrating hypotheses developed in behavioral ecology to account for individual decisions. This allows development of models of population and metapopulation dynamics that explicitly incorporate ecological and evolutionary processes.

Hierarchical modeling of an invasive spread: the Eurasian Collared-Dove Streptopelia decaocto in the United States.

Invasive species are regularly claimed as the second threat to biodiversity. To apply a relevant response to the potential consequences associated with invasions (e.g., emphasize management efforts to prevent new colonization or to eradicate the species in places where it has already settled), it is essential to understand invasion mechanisms and dynamics. Quantifying and understanding what influences rates of spatial spread is a key research area for invasion theory. In this paper, we develop a model to account for occupancy dynamics of an invasive species. Our model extends existing models to accommodate several elements of invasive processes; we chose the framework of hierarchical modeling to assess site occupancy status during an invasion. First, we explicitly accounted for spatial structure and how distance among sites and position relative to one another affect the invasion spread. In particular, we accounted for the possibility of directional propagation and provided a way of estimating the direction of this possible spread. Second, we considered the influence of local density on site occupancy. Third, we decided to split the colonization process into two subprocesses, initial colonization and recolonization, which may be ground-breaking because these subprocesses may exhibit different relationships with environmental variations (such as density variation) or colonization history (e.g., initial colonization might facilitate further colonization events). Finally, our model incorporates imperfection in detection, which might be a source of substantial bias in estimating population parameters. We focused on the case of the Eurasian Collared-Dove (Streptopelia decaocto) and its invasion of the United States since its introduction in the early 1980s, using data from the North American BBS (Breeding Bird Survey). The Eurasian Collared-Dove is one of the most successful invasive species, at least among terrestrial vertebrates. Our model provided estimation of the spread direction consistent with empirical observations. Site persistence probability exhibits a quadratic response to density. We also succeeded at detecting differences in the relationship between density and initial colonization vs. recolonization probabilities. We provide a map of sites that may be colonized in the future as an example of possible practical application of our work.

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.

The risk of flawed inference in evolutionary studies when detectability is less than one.

Addressing evolutionary questions in the wild remains a challenge. It is best done by monitoring organisms from birth to death, which is very difficult in part because individuals may or may not be resighted or recaptured. Although the issue of uncertain detection has long been acknowledged in ecology and conservation biology, in evolutionary studies of wild populations it is often assumed that detectability is perfect. We argue that this assumption may lead to flawed inference. We demonstrate that the form of natural selection acting on body mass of sociable weavers is altered and that the rate of senescence of roe deer is underestimated when not accounting for a value of detectability that is less than one. Because mark-recapture models provide an explicit way to integrate and reliably model the detection process, we strongly recommend their use to address questions in evolutionary biology.

Influence of food availability on demography and local population dynamics in a long-lived seabird.

Few studies have addressed the effects of food availability as a proximate factor affecting local adult survival in long-lived organisms and their consequences at local population dynamics. We used capture-recapture analysis of resightings of 10 birth cohorts of ringed Audouin's gulls, Larus audouinii, to estimate adult survival and dispersal (both emigration and immigration). For the first time, permanent emigration (the transient effect in capture-recapture analysis) was modelled for the whole population and not only for the newly marked birds. Gulls exploit to a large extent fishes discarded from trawlers, and a trawling moratorium established since 1991 has decreased food supply for the colony. This was used as a natural experiment of food availability to assess its effects on adult survival and emigration. These and other demographic parameters were used in a projection modelling to assess the probabilities of extinction of the colony under two scenarios of lower and higher food availability. Food availability (together with the age of individuals) influenced emigration probabilities, but not adult survival, which was estimated at 0.91 (s.e. = 0.02). When food was in shorter supply during the chick-rearing period, emigration was very high (ca. 65%) for younger breeders, although this rate decreased sharply with age. Probabilities of extinction were very high when food availability was low, and when environmental stochasticity was introduced, and only stochastic immigration from the outside seemed to prevent extinction. The results highlight the importance of dispersal processes in the population dynamics of long-lived organisms.

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.