Individual life histories: neither slow nor fast, just diverse.

The slow-fast continuum is a commonly used framework to describe variation in life-history strategies across species. Individual life histories have also been assumed to follow a similar pattern, especially in the pace-of-life syndrome literature. However, whether a slow-fast continuum commonly explains life-history variation among individuals within a population remains unclear. Here, we formally tested for the presence of a slow-fast continuum of life histories both within populations and across species using detailed long-term individual-based demographic data for 17 bird and mammal species with markedly different life histories. We estimated adult lifespan, age at first reproduction, annual breeding frequency, and annual fecundity, and identified the main axes of life-history variation using principal component analyses. Across species, we retrieved the slow-fast continuum as the main axis of life-history variation. However, within populations, the patterns of individual life-history variation did not align with a slow-fast continuum in any species. Thus, a continuum ranking individuals from slow to fast living is unlikely to shape individual differences in life histories within populations. Rather, individual life-history variation is likely idiosyncratic across species, potentially because of processes such as stochasticity, density dependence, and individual differences in resource acquisition that affect species differently and generate non-generalizable patterns across species.

Winter mortality of a passerine bird increases following hotter summers and during winters with higher maximum temperatures.

Climate change may influence animal population dynamics through reproduction and mortality. However, attributing changes in mortality to specific climate variables is challenging because the exact time of death is usually unknown in the wild. Here, we investigated climate effects on adult mortality in Australian superb fairy-wrens (Malurus cyaneus). Over a 27-year period, mortality outside the breeding season nearly doubled. This nonbreeding season mortality increased with lower minimum (night-time) and higher maximum (day-time) winter temperatures and with higher summer heat wave intensity. Fine-scale analysis showed that higher mortality in a given week was associated with higher maxima 2 weeks prior and lower minima in the current fortnight, indicating costs of temperature drops. Increases in summer heat waves and in winter maximum temperatures collectively explained 62.6% of the increase in mortality over the study period. Our results suggest that warming climate in both summer and winter can adversely affect survival, with potentially substantial population consequences.

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.

Bird populations most exposed to climate change are less sensitive to climatic variation.

The phenology of many species shows strong sensitivity to climate change; however, with few large scale intra-specific studies it is unclear how such sensitivity varies over a species' range. We document large intra-specific variation in phenological sensitivity to temperature using laying date information from 67 populations of two co-familial European songbirds, the great tit (Parus major) and blue tit (Cyanistes caeruleus), covering a large part of their breeding range. Populations inhabiting deciduous habitats showed stronger phenological sensitivity than those in evergreen and mixed habitats. However, populations with higher sensitivity tended to have experienced less rapid change in climate over the past decades, such that populations with high phenological sensitivity will not necessarily exhibit the strongest phenological advancement. Our results show that to effectively assess the impact of climate change on phenology across a species' range it will be necessary to account for intra-specific variation in phenological sensitivity, climate change exposure, and the ecological characteristics of a population.

Warming temperatures drive at least half of the magnitude of long-term trait changes in European birds.

SignificanceClimate change is impacting wild populations, but its relative importance compared to other causes of change is still unclear. Many studies assume that changes in traits primarily reflect effects of climate change, but this assumption is rarely tested. We show that in European birds global warming was likely the single most important contributor to temporal trends in laying date, body condition, and offspring number. However, nontemperature factors were also important and acted in the same direction, implying that attributing temporal trends solely to rising temperatures overestimates the impact of climate warming. Differences among species in the amount of trait change were predominantly determined by these nontemperature effects, suggesting that species differences are not due to variation in sensitivity to temperature.

The demographic causes of population change vary across four decades in a long-lived shorebird.

Understanding which factors cause populations to decline begins with identifying which parts of the life cycle, and which vital rates, have changed over time. However, in a world where humans are altering the environment both rapidly and in different ways, the demographic causes of decline likely vary over time. Identifying temporal variation in demographic causes of decline is crucial to assure that conservation actions target current and not past threats. However, this has rarely been studied as it requires long time series. Here we investigate how the demography of a long-lived shorebird (the Eurasian Oystercatcher Haematopus ostralegus) has changed in the past four decades, resulting in a shift from stable dynamics to strong declines (-9% per year), and recently back to a modest decline. Since individuals of this species are likely to respond differently to environmental change, we captured individual heterogeneity through three state variables: age, breeding status, and lay date (using integral projection models). Timing of egg-laying explained significant levels of variation in reproduction, with a parabolic relationship of maximal productivity near the average lay date. Reproduction explained most variation in population growth rates, largely due to poor nest success and hatchling survival. However, the demographic causes of decline have also been in flux over the last three decades: hatchling survival was low in the 2000s but improved in the 2010s, while adult survival declined in the 2000s and remains low today. Overall, the joint action of several key demographic variables explain the decline of the oystercatcher, and improvements in a single vital rate cannot halt the decline. Conservations actions will thus need to address threats occurring at different stages of the oystercatcher's life cycle. The dynamic nature of the threat landscape is further supported by the finding that the average individual no longer has the highest performance in the population, and emphasizes how individual heterogeneity in vital rates can play an important role in modulating population growth rates. Our results indicate that understanding population decline in the current era requires disentangling demographic mechanisms, individual variability, and their changes over time.

GPS tracking data of Eurasian oystercatchers (Haematopusostralegus) from the Netherlands and Belgium.

We describe six datasets that contain GPS and accelerometer data of 202 Eurasian oystercatchers (Haematopusostralegus) spanning the period 2008-2021. Birds were equipped with GPS trackers in breeding and wintering areas in the Netherlands and Belgium. We used GPS trackers from the University of Amsterdam Bird Tracking System (UvA-BiTS) for several study purposes, including the study of space use during the breeding season, habitat use and foraging behaviour in the winter season, and impacts of human disturbance. To enable broader usage, all data have now been made open access. Combined, the datasets contain 6.0 million GPS positions, 164 million acceleration measurements and 7.0 million classified behaviour events (i.e., flying, walking, foraging, preening, and inactive). The datasets are deposited on the research repository Zenodo, but are also accessible on Movebank and as down-sampled occurrence datasets on the Global Biodiversity Information Facility (GBIF) and Ocean Biodiversity Information System (OBIS).

Conceptualizing and quantifying body condition using structural equation modelling: A user guide.

Body condition is an important concept in behaviour, evolution and conservation, commonly used as a proxy of an individual's performance, for example in the assessment of environmental impacts. Although body condition potentially encompasses a wide range of health state dimensions (nutritional, immune or hormonal status), in practice most studies operationalize body condition using a single (univariate) measure, such as fat storage. One reason for excluding additional axes of variation may be that multivariate descriptors of body condition impose statistical and analytical challenges. Structural equation modelling (SEM) is used in many fields to study questions relating multidimensional concepts, and we here explain how SEM is a useful analytical tool to describe the multivariate nature of body condition. In this 'Research Methods Guide' paper, we show how SEM can be used to resolve different challenges in analysing the multivariate nature of body condition, such as (a) variable reduction and conceptualization, (b) specifying the relationship of condition to performance metrics, (c) comparing competing causal hypothesis and (d) including many pathways in a single model to avoid stepwise modelling approaches. We illustrated the use of SEM on a real-world case study and provided R-code of worked examples as a learning tool. We compared the predictive power of SEM with conventional statistical approaches that integrate multiple variables into one condition variable: multiple regression and principal component analyses. We show that model performance on our dataset is higher when using SEM and led to more accurate and precise estimates compared to conventional approaches. We encourage researchers to consider SEM as a flexible framework to describe the multivariate nature of body condition and thus understand how it affects biological processes, thereby improving the value of body condition proxies for predicting organismal performance. Finally, we highlight that it can be useful for other multidimensional ecological concepts as well, such as immunocompetence, oxidative stress and environmental conditions.

Cross-lags and the unbiased estimation of life-history and demographic parameters.

Biological processes exhibit complex temporal dependencies due to the sequential nature of allocation decisions in organisms' life cycles, feedback loops and two-way causality. Consequently, longitudinal data often contain cross-lags: the predictor variable depends on the response variable of the previous time step. Although statisticians have warned that regression models that ignore such covariate endogeneity in time series are likely to be inappropriate, this has received relatively little attention in biology. Furthermore, the resulting degree of estimation bias remains largely unexplored. We use a graphical model and numerical simulations to understand why and how regression models that ignore cross-lags can be biased, and how this bias depends on the length and number of time series. Ecological and evolutionary examples are provided to illustrate that cross-lags may be more common than is typically appreciated and that they occur in functionally different ways. We show that routinely used regression models that ignore cross-lags are asymptotically unbiased. However, this offers little relief, as for most realistically feasible lengths of time-series conventional methods are biased. Furthermore, collecting time series on multiple subjects-such as populations, groups or individuals-does not help to overcome this bias when the analysis focusses on within-subject patterns (often the pattern of interest). Simulations, a literature search and a real-world empirical example together suggest that approaches that ignore cross-lags are likely biased in the direction opposite to the sign of the cross-lag (e.g. towards detecting density dependence of vital rates and against detecting life-history trade-offs and benefits of group living). Next, we show that multivariate (e.g. structural equation) models can dynamically account for cross-lags, and simultaneously address additional bias induced by measurement error, but only if the analysis considers multiple time series. We provide guidance on how to identify a cross-lag and subsequently specify it in a multivariate model, which can be far from trivial. Our tutorials with data and R code of the worked examples provide step-by-step instructions on how to perform such analyses. Our study offers insights into situations in which cross-lags can bias analysis of ecological and evolutionary time series and suggests that adopting dynamical models can be important, as this directly affects our understanding of population regulation, the evolution of life histories and cooperation, and possibly many other topics. Determining how strong estimation bias due to ignoring covariate endogeneity has been in the ecological literature requires further study, also because it may interact with other sources of bias.

hiphop: Improved paternity assignment among close relatives using a simple exclusion method for biallelic markers.

Assignment of parentage with molecular markers is most difficult when the true parents have close relatives in the adult population. Here, we present an efficient solution to that problem by extending simple exclusion approaches to parentage analysis with single nucleotide polymorphic markers (SNPs). We augmented the previously published homozygote opposite test (hot), which counts mismatches due to the offspring and candidate parent having different homozygous genotypes, with an additional test. In this case, parents homozygous for the same SNP are incompatible with heterozygous offspring (i.e., "Homozygous Identical Parents, Heterozygous Offspring are Precluded": hiphop). We tested this approach in a cooperatively breeding bird, the superb fairy-wren, Malurus cyaneus, where rates of extra-pair paternity are exceptionally high, and where paternity assignment is challenging because breeding males typically have first-order adult relatives in their neighbourhood. Combining the tests and conditioning on the maternal genotype with a set of 1376 autosomal SNPs always allowed us to distinguish a single most likely sire from his relatives, and also to identify cases where the true sire must have been unsampled. In contrast, if just the hot test was used, we failed to identify a single most-likely sire in 2.5% of cases. Resampling enabled us to create guidelines for the number of SNPs required when first-order relatives coexist in the mating pool. Our method, implemented in the R package hiphop, therefore provides unambiguous parentage assignments even in systems with complex social organisation. We also identified a suite of Z- and W-linked SNPs that always identified sex correctly.

Fluctuating optimum and temporally variable selection on breeding date in birds and mammals.

Temporal variation in natural selection is predicted to strongly impact the evolution and demography of natural populations, with consequences for the rate of adaptation, evolution of plasticity, and extinction risk. Most of the theory underlying these predictions assumes a moving optimum phenotype, with predictions expressed in terms of the temporal variance and autocorrelation of this optimum. However, empirical studies seldom estimate patterns of fluctuations of an optimum phenotype, precluding further progress in connecting theory with observations. To bridge this gap, we assess the evidence for temporal variation in selection on breeding date by modeling a fitness function with a fluctuating optimum, across 39 populations of 21 wild animals, one of the largest compilations of long-term datasets with individual measurements of trait and fitness components. We find compelling evidence for fluctuations in the fitness function, causing temporal variation in the magnitude, but not the direction of selection. However, fluctuations of the optimum phenotype need not directly translate into variation in selection gradients, because their impact can be buffered by partial tracking of the optimum by the mean phenotype. Analyzing individuals that reproduce in consecutive years, we find that plastic changes track movements of the optimum phenotype across years, especially in bird species, reducing temporal variation in directional selection. This suggests that phenological plasticity has evolved to cope with fluctuations in the optimum, despite their currently modest contribution to variation in selection.

Integrating Fitness Components Reveals That Survival Costs Outweigh Other Benefits and Costs of Group Living in Two Closely Related Species.

Group living can be beneficial when individuals reproduce or survive better in the presence of others, but, simultaneously, there might be costs due to competition for resources. Positive and negative effects on various fitness components might thus counteract each other, so integration is essential to determine their overall effect. Here, we investigated how an integrated fitness measure (reproductive values [RVs]) based on six fitness components varied with group size among group members in cooperatively breeding red-winged and superb fairy wrens (Malurus elegans and Malurus cyaneus, respectively). Despite life-history differences between the species, patterns of RVs were similar, suggesting that the same behavioral mechanisms are important. Group living reduced RVs for dominant males, but for other group members, this was true only in large groups. Decomposition analyses showed that our integrated fitness proxy was most strongly affected by group size effects on survival and was amplified through carryover effects between years. Our study shows that integrative consideration of fitness components and subsequent decomposition analysis provide much needed insights into the key behavioral mechanisms shaping the costs and benefits of group living. Such attribution is crucial if we are to synthesize the relative importance of the myriad group size costs and benefits currently reported in the literature.

Rapid plastic breeding response to rain matches peak prey abundance in a tropical savanna bird.

Changes in climate are shifting the timing of life cycle events in the natural world. Compared to northern temperate areas, these effects are relatively poorly understood in tropical and southern regions, where there is limited information on how timing of breeding and food availability are affected by climatic factors, and where patterns of breeding activity are more unpredictable within and between years. Combining a new statistical modelling approach with 5 years of continuous individual-based monitoring of a monsoonal tropical insectivorous bird, we quantified (a) the proximate climatic drivers at two trophic levels: timing of breeding and abundance of arthropod prey; (b) the effect of climate variation on reproductive output and (c) the role of individual plasticity. Rainfall was identified as the main determinant of phenology at both trophic levels. Throughout the year, likelihood of egg laying increased very rapidly in response to even small amounts of rain during the preceding 0-3 weeks. Adult body mass and male sperm storage also increased rapidly after rain, suggesting high breeding preparedness. Additionally, females were flexible, since they were more likely to nest whether their previous attempt was longer ago and unsuccessful. Arthropod abundance also increased after rainfall, but more slowly, with a peak around 10 weeks. Therefore, the peak food availability coincided with the presence of dependent fledglings. Fitness benefits of nesting after more rain appeared to be linked to offspring quantity rather than quality: nest attempts following higher rainfall produced larger clutches, but showed no improvement in nestling mass or relative fledging success. The response of clutch size to rainfall was plastic, since repeated sampling showed that individual females laid larger clutches after more rain, possibly mediated by improved body mass. Rapid, individually flexible breeding in response to rainfall and slower increase in arthropod abundance also as a response to rainfall, might buffer insectivorous species living in tropical seasonal environments from climate change-induced phenological trophic mismatches.

Autumn bird migration phenology: A potpourri of wind, precipitation and temperature effects.

Climate change has caused a clear and univocal trend towards advancement in spring phenology. Changes in autumn phenology are much more diverse, with advancement, delays, and 'no change' all occurring frequently. For migratory birds, patterns in autumn migration phenology trends have been identified based on ecological and life-history traits. Explaining interspecific variation has nevertheless been challenging, and the underlying mechanisms have remained elusive. Radar studies on non-species-specific autumn migration intensity have repeatedly suggested that there are strong links with weather. In long-term species-specific studies, the variance in autumn migration phenology explained by weather has, nevertheless, been rather low, or a relationship was even lacking entirely. We performed a spatially explicit time window analysis of weather effects on mean autumn passage of four trans-Saharan and six intra-European passerines to gain insights into this apparent contradiction. We analysed data from standardized daily captures at the Heligoland island constant-effort site (Germany), in combination with gridded daily temperature, precipitation and wind data over a 55-year period (1960-2014), across northern Europe. Weather variables at the breeding and stopover grounds explained up to 80% of the species-specific interannual variability in autumn passage. Overall, wind conditions were most important. For intra-European migrants, wind was even twice as important as either temperature or precipitation, and the pattern also held in terms of relative contributions of each climate variable to the temporal trends in autumn phenology. For the trans-Saharan migrants, however, the pattern of relative trend contributions was completely reversed. Temperature and precipitation had strong trend contributions, while wind conditions had only a minor impact because they did not show any strong temporal trends. As such, understanding species-specific effects of climate on autumn phenology not only provides unique insights into each species' ecology but also how these effects shape the observed interspecific heterogeneity in autumn phenological trends.

Adaptive responses of animals to climate change are most likely insufficient.

Biological responses to climate change have been widely documented across taxa and regions, but it remains unclear whether species are maintaining a good match between phenotype and environment, i.e. whether observed trait changes are adaptive. Here we reviewed 10,090 abstracts and extracted data from 71 studies reported in 58 relevant publications, to assess quantitatively whether phenotypic trait changes associated with climate change are adaptive in animals. A meta-analysis focussing on birds, the taxon best represented in our dataset, suggests that global warming has not systematically affected morphological traits, but has advanced phenological traits. We demonstrate that these advances are adaptive for some species, but imperfect as evidenced by the observed consistent selection for earlier timing. Application of a theoretical model indicates that the evolutionary load imposed by incomplete adaptive responses to ongoing climate change may already be threatening the persistence of species.

Comment on "Global pattern of nest predation is disrupted by climate change in shorebirds".

Kubelka et al (Reports, 9 November 2018, p. 680) claim that climate change has disrupted patterns of nest predation in shorebirds. They report that predation rates have increased since the 1950s, especially in the Arctic. We describe methodological problems with their analyses and argue that there is no solid statistical support for their claims.

Habitat selection can reduce effects of extreme climatic events in a long-lived shorebird.

Changes in the frequency of extreme climatic events (ECEs) can have profound impacts on individual fitness by degrading habitat quality. Organisms may respond to such changes through habitat selection, favouring those areas less affected by ECEs; however, documenting habitat selection in response to ECEs is difficult in the wild due to the rarity of such events and the long-term biological data required. Sea level rise and changing weather patterns over the past decades have led to an increase in the frequency of coastal flooding events, with serious consequences for ground nesting shorebirds. Shorebirds therefore present a useful natural study system to understand habitat selection as a response to ECEs. We used a 32-year study of the Eurasian oystercatcher (Haematopus ostralegus) to investigate whether habitat selection can lead to an increase in nest elevation and minimize the impacts of coastal flooding. The mean nest elevation of H. ostralegus has increased during the last three decades. We hypothesized that this change has been driven by changes in H. ostralegus territory settlement patterns over time. We compared various possible habitat selection cues to understand what information H. ostralegus might use to inform territory settlement. There was a clear relationship between elevation and territory settlement in H. ostralegus. In early years, settlements were more likely at low elevations but in more recent years the likelihood of settlement was similar between high and low elevation areas. Territory settlement was associated with conspecific fledgling output and conspecific density. Settlement was more likely in areas of high density and areas with high fledgling output. This study shows that habitat selection can minimize the effects of increasingly frequent ECEs. However, it seems unlikely that the changes we observe will fully alleviate the consequences of anthropogenic climate change. Rates of nest elevation increase were insufficient to track current increases in maximum high tide (0.5 vs. 0.8 cm/year). Furthermore, habitat selection cues that rely on information from previous breeding seasons (e.g. conspecific fledgling output) may become ineffective as ECEs become more frequent and environmental predictability is diminished.

Indirect fitness benefits through extra-pair mating are large for an inbred minority, but cannot explain widespread infidelity among red-winged fairy-wrens.

Extra-pair paternity (EPP) has been suggested to improve the genetic quality of offspring, but evidence has been equivocal. Benefits of EPP may be only available to specific individuals or under certain conditions. Red-winged fairy-wrens have extremely high levels of EPP, suggesting fitness benefits might be large and available to most individuals. Furthermore, extreme philopatry commonly leads to incestuous social pairings, so inbreeding avoidance may be an important selection pressure. Here, we quantified the fitness benefits of EPP under varying conditions and across life-stages. Extra-pair offspring (EPO) did not appear to have higher fitness than within-pair offspring (WPO), neither in poor years nor in the absence of helpers-at-the-nest. However, EPP was beneficial for closely related social pairs, because inbred WPO suffered an overall 75% reduction in fitness. Inbreeding depression was nonlinear and reduced nestling body condition, first year survival and reproductive success. Our comprehensive study indicates that EPP should be favored for the 17% of females paired incestuously, but cannot explain the widespread infidelity in this species. Furthermore, our finding that fitness benefits of EPP only become apparent for a small part of the population could potentially explain the apparent absence of fitness differences in population wide comparisons of EPO and WPO.

High intra-specific variation in avian body condition responses to climate limits generalisation across species.

It is generally assumed that populations of a species will have similar responses to climate change, and thereby that a single value of sensitivity will reflect species-specific responses. However, this assumption is rarely systematically tested. High intraspecific variation will have consequences for identifying species- or population-level traits that can predict differences in sensitivity, which in turn can affect the reliability of projections of future climate change impacts. We investigate avian body condition responses to changes in six climatic variables and how consistent and generalisable these responses are both across and within species, using 21 years of data from 46 common passerines across 80 Dutch sites. We show that body condition decreases with warmer spring/early summer temperatures and increases with higher humidity, but other climate variables do not show consistent trends across species. In the future, body condition is projected to decrease by 2050, mainly driven by temperature effects. Strikingly, populations of the same species generally responded just as differently as populations of different species implying that a single species signal is not meaningful. Consequently, species-level traits did not explain interspecific differences in sensitivities, rather population-level traits were more important. The absence of a clear species signal in body condition responses implies that generalisation and identifying species for conservation prioritisation is problematic, which sharply contrasts conclusions of previous studies on the climate sensitivity of phenology.

Multiple hypotheses explain variation in extra-pair paternity at different levels in a single bird family.

Extra-pair paternity (EPP), where offspring are sired by a male other than the social male, varies enormously both within and among species. Trying to explain this variation has proved difficult because the majority of the interspecific variation is phylogenetically based. Ideally, variation in EPP should be investigated in closely related species, but clades with sufficient variation are rare. We present a comprehensive multifactorial test to explain variation in EPP among individuals in 20 populations of nine species over 89 years from a single bird family (Maluridae). Females had higher EPP in the presence of more helpers, more neighbours or if paired incestuously. Furthermore, higher EPP occurred in years with many incestuous pairs, populations with many helpers and species with high male density or in which males provide less care. Altogether, these variables accounted for 48% of the total and 89% of the interspecific and interpopulation variation in EPP. These findings indicate why consistent patterns in EPP have been so challenging to detect and suggest that a single predictor is unlikely to account for the enormous variation in EPP across levels of analysis. Nevertheless, it also shows that existing hypotheses can explain the variation in EPP well and that the density of males in particular is a good predictor to explain variation in EPP among species when a large part of the confounding effect of phylogeny is excluded.