Evolution of chain migration in an aerial insectivorous bird, the common swift Apus apus.

Spectacular long-distance migration has evolved repeatedly in animals enabling exploration of resources separated in time and space. In birds, these patterns are largely driven by seasonality, cost of migration, and asymmetries in competition leading most often to leapfrog migration, where northern breeding populations winter furthest to the south. Here, we show that the highly aerial common swift Apus apus, spending the nonbreeding period on the wing, instead exhibits a rarely found chain migration pattern, where the most southern breeding populations in Europe migrate to wintering areas furthest to the south in Africa, whereas the northern populations winter to the north. The swifts concentrated in three major areas in sub-Saharan Africa during the nonbreeding period, with substantial overlap of nearby breeding populations. We found that the southern breeding swifts were larger, raised more young, and arrived to the wintering areas with higher seasonal variation in greenness (Normalized Difference Vegetation Index) earlier than the northern breeding swifts. This unusual chain migration pattern in common swifts is largely driven by differential annual timing and we suggest it evolves by prior occupancy and dominance by size in the breeding quarters and by prior occupancy combined with diffuse competition in the winter.

Demographic routes to variability and regulation in bird populations.

There is large interspecific variation in the magnitude of population fluctuations, even among closely related species. The factors generating this variation are not well understood, primarily because of the challenges of separating the relative impact of variation in population size from fluctuations in the environment. Here, we show using demographic data from 13 bird populations that magnitudes of fluctuations in population size are mainly driven by stochastic fluctuations in the environment. Regulation towards an equilibrium population size occurs through density-dependent mortality. At small population sizes, population dynamics are primarily driven by environment-driven variation in recruitment, whereas close to the carrying capacity K, variation in population growth is more strongly influenced by density-dependent mortality of both juveniles and adults. Our results provide evidence for the hypothesis proposed by Lack that population fluctuations in birds arise from temporal variation in the difference between density-independent recruitment and density-dependent mortality during the non-breeding season.

Predator-vole interactions in Northern Europe: the role of small mustelids revised.

The cyclic population dynamics of vole and predator communities is a key phenomenon in northern ecosystems, and it appears to be influenced by climate change. Reports of collapsing rodent cycles have attributed the changes to warmer winters, which weaken the interaction between voles and their specialist subnivean predators. Using population data collected throughout Finland during 1986-2011, we analyse the spatio-temporal variation in the interactions between populations of voles and specialist, generalist and avian predators, and investigate by simulations the roles of the different predators in the vole cycle. We test the hypothesis that vole population cyclicity is dependent on predator-prey interactions during winter. Our results support the importance of the small mustelids for the vole cycle. However, weakening specialist predation during winters, or an increase in generalist predation, was not associated with the loss of cyclicity. Strengthening of delayed density dependence coincided with strengthening small mustelid influence on the summer population growth rates of voles. In conclusion, a strong impact of small mustelids during summers appears highly influential to vole population dynamics, and deteriorating winter conditions are not a viable explanation for collapsing small mammal population cycles.

Europe-wide dampening of population cycles in keystone herbivores.

Suggestions of collapse in small herbivore cycles since the 1980s have raised concerns about the loss of essential ecosystem functions. Whether such phenomena are general and result from extrinsic environmental changes or from intrinsic process stochasticity is currently unknown. Using a large compilation of time series of vole abundances, we demonstrate consistent cycle amplitude dampening associated with a reduction in winter population growth, although regulatory processes responsible for cyclicity have not been lost. The underlying syndrome of change throughout Europe and grass-eating vole species suggests a common climatic driver. Increasing intervals of low-amplitude small herbivore population fluctuations are expected in the future, and these may have cascading impacts on trophic webs across ecosystems.

Nonlinear effects of climate on boreal rodent dynamics: mild winters do not negate high-amplitude cycles.

Small rodents are key species in many ecosystems. In boreal and subarctic environments, their importance is heightened by pronounced multiannual population cycles. Alarmingly, the previously regular rodent cycles appear to be collapsing simultaneously in many areas. Climate change, particularly decreasing snow quality or quantity in winter, is hypothesized as a causal factor, but the evidence is contradictory. Reliable analysis of population dynamics and the influence of climate thereon necessitate spatially and temporally extensive data. We combined data on vole abundances and climate, collected at 33 locations throughout Finland from 1970 to 2011, to test the hypothesis that warming winters are causing a disappearance of multiannual vole cycles. We predicted that vole population dynamics exhibit geographic and temporal variation associated with variation in climate; reduced cyclicity should be observed when and where winter weather has become milder. We found that the temporal patterns in cyclicity varied between climatically different regions: a transient reduction in cycle amplitude in the coldest region, low-amplitude cycles or irregular dynamics in the climatically intermediate regions, and strengthening cyclicity in the warmest region. Our results did not support the hypothesis that mild winters are uniformly leading to irregular dynamics in boreal vole populations. Long and cold winters were neither a prerequisite for high-amplitude multiannual cycles, nor were mild winters with reduced snow cover associated with reduced winter growth rates. Population dynamics correlated more strongly with growing season than with winter conditions. Cyclicity was weakened by increasing growing season temperatures in the cold, but strengthened in the warm regions. High-amplitude multiannual vole cycles emerge in two climatic regimes: a winter-driven cycle in cold, and a summer-driven cycle in warm climates. Finally, we show that geographic climatic gradients alone may not reliably predict biological responses to climate change.

Selection on plasticity of seasonal life-history traits using random regression mixed model analysis.

Theory considers the covariation of seasonal life-history traits as an optimal reaction norm, implying that deviating from this reaction norm reduces fitness. However, the estimation of reaction-norm properties (i.e., elevation, linear slope, and higher order slope terms) and the selection on these is statistically challenging. We here advocate the use of random regression mixed models to estimate reaction-norm properties and the use of bivariate random regression to estimate selection on these properties within a single model. We illustrate the approach by random regression mixed models on 1115 observations of clutch sizes and laying dates of 361 female Ural owl Strix uralensis collected over 31 years to show that (1) there is variation across individuals in the slope of their clutch size-laying date relationship, and that (2) there is selection on the slope of the reaction norm between these two traits. Hence, natural selection potentially drives the negative covariance in clutch size and laying date in this species. The random-regression approach is hampered by inability to estimate nonlinear selection, but avoids a number of disadvantages (stats-on-stats, connecting reaction-norm properties to fitness). The approach is of value in describing and studying selection on behavioral reaction norms (behavioral syndromes) or life-history reaction norms. The approach can also be extended to consider the genetic underpinning of reaction-norm properties.

The impact of climate and cyclic food abundance on the timing of breeding and brood size in four boreal owl species.

The ongoing climate change has improved our understanding of how climate affects the reproduction of animals. However, the interaction between food availability and climate on breeding has rarely been examined. While it has been shown that breeding of boreal birds of prey is first and foremost determined by prey abundance, little information exists on how climatic conditions influence this relationship. We studied the joint effects of main prey abundance and ambient weather on timing of breeding and reproductive success of two smaller (pygmy owl Glaucidium passerinum and Tengmalm's owl Aegolius funereus) and two larger (tawny owl Strix aluco and Ural owl Strix uralensis) avian predator species using long-term nation-wide datasets during 1973-2004. We found no temporal trend either in vole abundance or in hatching date and brood size of any studied owl species. In the larger species, increasing late winter or early spring temperature advanced breeding at least as much as did high autumn abundance of prey (voles). Furthermore, increasing snow depth delayed breeding of the largest species (Ural owl), presumably by reducing the availability of voles. Brood size was strongly determined by spring vole abundance in all four owl species. These results show that climate directly affects the breeding performance of vole-eating boreal avian predators much more than previously thought. According to earlier studies, small-sized species should advance their breeding more than larger species in response to increasing temperature. However, we found an opposite pattern, with larger species being more sensitive to temperature. We argue that this pattern is caused by a difference in the breeding tactics of larger mostly capital breeding and smaller mostly income breeding owl species.

Senescence rates are determined by ranking on the fast-slow life-history continuum.

Comparative analyses of survival senescence by using life tables have identified generalizations including the observation that mammals senesce faster than similar-sized birds. These generalizations have been challenged because of limitations of life-table approaches and the growing appreciation that senescence is more than an increasing probability of death. Without using life tables, we examine senescence rates in annual individual fitness using 20 individual-based data sets of terrestrial vertebrates with contrasting life histories and body size. We find that senescence is widespread in the wild and equally likely to occur in survival and reproduction. Additionally, mammals senesce faster than birds because they have a faster life history for a given body size. By allowing us to disentangle the effects of two major fitness components our methods allow an assessment of the robustness of the prevalent life-table approach. Focusing on one aspect of life history - survival or recruitment - can provide reliable information on overall senescence.

Single-generation estimates of individual fitness as proxies for long-term genetic contribution.

Individual fitness is a central evolutionary concept, but the question of how it should be defined in empirical studies of natural selection remains contentious. Using founding cohorts from long-term population studies of two species of individually marked birds (collared flycatcher Ficedula albicollis and Ural owl Strix uralensis), we compared a rate-sensitive (lambdaind) and a rate-insensitive (lifetime reproductive success [LRS]) estimate of individual fitness with an estimate of long-term genetic fitness. The latter was calculated as the number of gene copies present in the population after more than two generations, as estimated by tracing genetic lineages and accounting for the fact that populations were not completely closed. When counting fledglings, rate-insensitive estimates of individual fitness correlated better than rate-sensitive estimates with estimated long-term genetic contribution. When counting recruits, both classes of estimates performed equally well. The results support the contention that simple, rate-insensitive measures of fitness, such as LRS, provide a valid and good estimate of fitness in evolutionary studies of natural populations.

Supplementary fed Ural owls increase their reproductive output with a one year time lag.

Life-history components may be food-limited. We supplemented food to 18 Ural owl, Strix uralensis, nests during the nestling period. Food supplementation led to a higher somatic condition in the female parent, but effects in males were moderate. Parents delivered less food to fed nests than to control nests. Offspring survival and fledging condition did not differ between control and fed nests. In the season following food supplementation, fed pairs bred 1 week earlier than control pairs and, coupled to this advance in laying date, fed pairs produced 0.6 eggs more than control pairs. This is the first evidence that food limitation in the current season may constrain next season's reproduction. Such carry-over effects of food-limitation may have important consequences for population dynamics.

Ural owl sex allocation and parental investment under poor food conditions.

Parents are expected to overproduce the less costly sex under poor food conditions. The previously regular 3-year cycle in the abundance of voles, the main prey of the Ural owl, Strix uralensis, temporarily disappeared in 1999-2001. We studied Ural owls' parental feeding investment and sex allocation during these poor-quality years. We sexed hatchlings and embryos in unhatched eggs of all 131 broods produced during these years. Population wide, the owls produced significantly more males (56%). The parental food investment in the brood was estimated by sorting out the prey remains in the bottom of nest boxes. Food delivered to 83 broods without chick mortality showed no clear sex-specific investment. Nestling mortality was equal in both sexes. Thus, evidence for an investment-driven sex allocation is weak. Neither laying date, brood size nor the female's condition correlated with offspring sex ratios. In these poor years, parents provided less food per chick and the fledgling weight of daughters was reduced more than the weight of sons compared with years of high food abundance (1983 and 1986). We discuss, in relation to published studies, the possibility of a sex-allocation scenario where, under poor food conditions, a daughter's long-term fitness is reduced more than a son's.

Cyclic variation in seasonal recruitment and the evolution of the seasonal decline in Ural owl clutch size.

Plastic life-history traits can be viewed as adaptive responses to environmental conditions, described by a reaction norm. In birds, the decline in clutch size with advancing laying date has been viewed as a reaction norm in response to the parent's own (somatic or local environmental) condition and the seasonal decline in its offspring's reproductive value. Theory predicts that differences in the seasonal recruitment are mirrored in the seasonal decrease in clutch size. We tested this prediction in the Ural owl. The owl's main prey, voles, show a cycle of low, increase and peak phases. Recruitment probability had a humped distribution in both increase and peak phases. Average recruitment probability was two to three times higher in the increase phase and declined faster in the latter part of the season when compared with the peak phase. Clutch size decreased twice as steep in the peak (0.1 eggs day-1) as in the increase phase (0.05 eggs day-1). This result appears to refute theoretical predictions of seasonal clutch size declines. However, a re-examination of current theory shows that the predictions of modelling are less robust to details of seasonal condition accumulation in birds than originally thought. The observed pattern can be predicted, assuming specifically shaped seasonal increases in condition across individuals.

Reproductive Effort and Reproductive Values in Periodic Environments.

Life-history theory concerns the optimal spread of reproduction over an organism's life span. In variable environments, there may be extrinsic differences between breeding periods within an organism's life, affecting both offspring and parent and giving rise to intergenerational trade-offs. Such trade-offs are often discussed in terms of reproductive value for parent and offspring. Here, we consider parental life-history optimization in response to varying offspring values of a population regulated by territoriality, where the quality of the environment varies periodically. Periods are interpreted as either within-year (seasonality) or between-years variation (cyclicity). The evolutionarily stable strategy in a general model with two-phased periodicity in the environment can generate either higher or lower effort in the more favorable of the two phases; hence knowing survival prospects of offspring does not suffice for predicting reproductive effort-the future of all descendants and the parent must be tracked. We also apply our method to data on the Ural owl Strix uralensis, a species preying on cyclically fluctuating voles. The observed dynamics are best predicted by assuming delayed reproductive costs and Type II functional response. Accounting for varying offspring values can lead to cases where both reproductive effort and recruitment of offspring are higher in the phase when voles are not maximally abundant, a pattern supported by our data.