Identifying the paths of climate effects on population dynamics: dynamic and multilevel structural equation model around the annual cycle.

How environmental factors influence population dynamics in long-distance migrants is complicated by the spatiotemporal diversity of the environment the individuals experience during the annual cycle. The effects of weather on several different aspects of life history have been well studied, but a better understanding is needed on how weather affects population dynamics through the different associated traits. We utilise 77 years of data from pied flycatcher (Ficedula hypoleuca), to identify the most relevant climate signals associated with population growth rate. The strongest signals on population growth were observed from climate during periods when the birds were not present in the focal location. The population decline was associated with increasing precipitation in the African non-breeding quarters in the autumn (near the arrival of migrants) and with increasing winter temperature along the migration route (before migration). The number of fledglings was associated positively with increasing winter temperature in non-breeding area and negatively with increasing winter temperature in Europe. These possible carry-over effects did not arise via timing of breeding or clutch size but the exact mechanism remains to be revealed in future studies. High population density and low fledgling production were the intrinsic factors reducing the breeding population. We conclude that weather during all seasons has the potential to affect the reproductive success or population growth rate of this species. Our results show how weather can influence the population dynamics of a migratory species through multiple pathways, even at times of the annual cycle when the birds are in a different location than the climate signal.

Weather and biotic interactions as determinants of seasonal shifts in abundance measured through nest-box occupancy in the Siberian flying squirrel.

It is much debated whether the direct effects of weather or biotic interactions determine species' responses to climate change. For example, an important biotic factor for herbivores in northern ecosystems is the availability of winter food. If the food availability changes because of the changing climate, it likely has major impact on the abundance of herbivores. To evaluate this, we need to know the relative roles of weather and biotic interactions, such as food availability and risk of predation, for the species. Here, we utilize long-term data on nest-box occupancy by Siberian flying squirrels (Pteromys volans) in Finland during 2002-2018. We built binary models with nest-box occupancy in different seasons as a response variable. Weather, winter food (tree mast), and predator presence (the Ural owl, Strix uralensis) modified seasonal nest-box occupancy patterns of the flying squirrel. However, the effect of weather was only important in the summer. The negative effect of predators was clear for adults but, surprisingly, not for overwinter survival of apparent juveniles. Considering the relative importance of different factors, winter food availability had a clear positive effect in each season. Our study supports the view that the effects of climate change mediate through multiple biotic interactions. In forest ecosystems, responses of masting trees to weather likely play an important role in species responses to climate change.

Within-season changes in habitat use of forest-dwelling boreal bats.

Bats utilize forests as roosting sites and feeding areas. However, it has not been documented how bats utilize these habitats in the boreal zone with methods afforded by recent technological advances. Forest structure and management practices can create a variety of three-dimensional habitats for organisms capable of flight, such as bats. Here, we study the presence of boreal bats in a forest forming a mosaic of different age classes, dominant tree species, canopy cover, soil fertility, and other environmental variables, throughout their active season in the summer using passive ultrasound detectors. Our results indicate a preference for mature forest by Eptesicus nilssonii and a pooled set of Myotis bats. Both groups of bats also showed temporal changes in their habitat use regarding forest age. In June and July, both groups occurred more often in mature than young forests, but from August onwards, the difference in occurrence became less evident in Myotis and disappeared completely in E. nilssonii. In addition, E. nilssonii was more often present in forests with low canopy cover, and its occurrence shifted from coniferous forests to deciduous forests during the season. The results reflect the within-season dynamics of bat communities and their ability to utilize different types of forest as environmental conditions change. Yet, the results most importantly emphasize the importance of mature forests to bat diversity and the need to conserve such environments in the boreal zone.

Large-scale spatial synchrony in red squirrel populations driven by a bottom-up effect.

Spatial synchrony between populations emerges from endogenous and exogenous processes, such as intra- and interspecific interactions and abiotic factors. Understanding factors contributing to synchronous population dynamics help to better understand what determines abundance of a species. This study focuses on spatial and temporal dynamics in the Eurasian red squirrel (Sciurus vulgaris) using snow-track data from Finland from 29 years. We disentangled the effects of bottom-up and top-down forces as well as environmental factors on population dynamics with a spatiotemporally explicit Bayesian hierarchical approach. We found red squirrel abundance to be positively associated with both the abundance of Norway spruce (Picea abies) cones and the predators, the pine marten (Martes martes) and the northern goshawk (Accipiter gentilis), probably due to shared habitat preferences. The results suggest that red squirrel populations are synchronized over remarkably large distances, on a scale of hundreds of kilometres, and that this synchrony is mainly driven by similarly spatially autocorrelated spruce cone crop. Our research demonstrates how a bottom-up effect can drive spatial synchrony in consumer populations on a very large scale of hundreds of kilometres, and also how an explicit spatiotemporal approach can improve model performance for fluctuating populations.

Population fluctuations and spatial synchrony in an arboreal rodent.

Climatic conditions, trophic links between species and dispersal may induce spatial synchrony in population fluctuations. Spatial synchrony increases the extinction risk of populations and, thus, it is important to understand how synchrony-inducing mechanisms affect populations already threatened by habitat loss and climate change. For many species, it is unclear how population fluctuations vary over time and space, and what factors potentially drive this variation. In this study, we focus on factors determining population fluctuations and spatial synchrony in the Siberian flying squirrel, Pteromys volans, using long-term monitoring data from 16 Finnish populations located 2-400 km apart. We found an indication of synchronous population dynamics on a large scale in flying squirrels. However, the synchrony was not found to be clearly related to distance between study sites because the populations seemed to be strongly affected by small-scale local factors. The regularity of population fluctuations varied over time. The fluctuations were linked to changes in winter precipitation, which has previously been linked to the reproductive success of flying squirrels. Food abundance (tree mast) and predator abundance were not related to population fluctuations in this study. We conclude that spatial synchrony was not unequivocally related to distance in flying squirrels, as has been observed in earlier studies for more abundant rodent species. Our study also emphasises the role of climate in population fluctuations and the synchrony of the species.

The effect of landscape structure on dispersal distances of the Eurasian red squirrel.

Landscape structure can affect dispersal and gene flow in a species. In urban areas, buildings, roads, and small habitat patches make the landscape highly fragmented and can inhibit movement and affect dispersal behavior. Similarly, in rural forested areas, large open areas, such as fields, may act as barriers to movement. We studied how landscape structure affects natal dispersal distances of Eurasian red squirrels (Sciurus vulgaris) in an urban area and a rural area in Finland, by monitoring juvenile red squirrels with radio telemetry. We observed extremely long dispersal distances-up to 16 km-in the rural study area, but shorter distances-on average only half a kilometer-in the urban study area. The landscape structure affected the eventual dispersal paths; in the rural landscape, dispersers favored spruce dominated areas and avoided fields along their dispersal route, although they occasionally even crossed wide fields. In the urban landscape, squirrels preferred areas with deciduous or coniferous trees. The movement steps made by dispersers were longer in the more hostile landscape compared to forested areas. Despite these effects on movement path, the landscape structure only had a minor effect on straight line dispersal distances moved from the natal nest. In other words, individuals moved longer distances and were likely to circumvent barriers in their path, but this did not affect how far they settled from their natal home. This result indicates that, although landscape structure has obvious effects on movement, it still may have only a small effect on other aspects of the population, for example, gene flow.

Predation risk landscape modifies flying and red squirrel nest site occupancy independently of habitat amount.

Habitat choice often entails trade-offs between food availability and predation risk. Understanding the distribution of individuals in space thus requires that both habitat characteristics and predation risk are considered simultaneously. Here, we studied the nest box use of two arboreal squirrels who share preferred habitat with their main predators. Nocturnal Ural owls (Strix uralensis) decreased occurrence of night-active flying squirrels (Pteromys volans) and diurnal goshawks (Accipiter gentilis) that of day-active red squirrels (Sciurus vulgaris). Unexpectedly, the amount of preferred habitat had no effect on nest box use, but, surprisingly, both squirrel species seemed to benefit from close proximity to agricultural fields and red squirrels to urban areas. We found no evidence of trade-off between settling in a high-quality habitat and avoiding predators. However, the amount of poor-quality young pine forests was lower in occupied sites where goshawks were present, possibly indicating habitat specific predation on red squirrels. The results suggest that erecting nest boxes for Ural owls should be avoided in the vicinity of flying squirrel territories in order to conserve the near threatened flying squirrels. Our results also suggest that flying squirrels do not always need continuous old forests, and hence the currently insufficient conservation practices could be improved with reasonable increases in the areas left untouched around their nests. The results of this study demonstrate the importance of taking into account both habitat requirements and predation risk as well as their interactive effects when modeling the occupancy of threatened animal species and planning their conservation.

Joint evolution of dispersal propensity and site selection in structured metapopulation models.

We propose a novel mathematical model for a metapopulation in which dispersal occurs on two levels: juvenile dispersal from the natal site is mandatory but it may take place either locally within the natal patch or globally between patches. Within each patch, individuals live in sites. Each site can be inhabited by at most one individual at a time and it may be of high or low quality. A disperser immigrates into a high-quality site whenever it obtains one, but it immigrates into a low-quality site only with a certain probability that depends on the time within the dispersal season. The vector of these low-quality-site-acceptance probabilities is the site-selection strategy of an individual. We derive a proxy for the invasion fitness in this model and study the joint evolution of long-distance-dispersal propensity and site-selection strategy. We focus on the way different ecological changes affect the evolutionary dynamics and study the interplay between global patch-to-patch dispersal and local site-selection. We show that ecological changes affect site-selection mainly via the severeness of competition for sites, which often leads to effects that may appear counterintuitive. Moreover, the metapopulation structure may result in extremely complex site-selection strategies and even in evolutionary cycles. The propensity for long-distance dispersal is mainly determined by the metapopulation-level ecological factors. It is, however, also strongly affected by the winter-survival of the site-holders within patches, which results in surprising non-monotonous effects in the evolution of site-selection due to interplay with long-distance dispersal. Altogether, our results give new additional support to the recent general conclusion that evolution of site-selection is often dominated by the indirect factors that take place via density-dependence, which means that evolutionary responses can rarely be predicted by intuition.

Multilevel landscape utilization of the Siberian flying squirrel: Scale effects on species habitat use.

Animals use and select habitat at multiple hierarchical levels and at different spatial scales within each level. Still, there is little knowledge on the scale effects at different spatial levels of species occupancy patterns. The objective of this study was to examine nonlinear effects and optimal-scale landscape characteristics that affect occupancy of the Siberian flying squirrel, Pteromys volans, in South- and Mid-Finland. We used presence-absence data (n = 10,032 plots of 9 ha) and novel approach to separate the effects on site-, landscape-, and regional-level occupancy patterns. Our main results were: landscape variables predicted the placement of population patches at least twice as well as they predicted the occupancy of particular sites; the clear optimal value of preferred habitat cover for species landscape-level abundance is a surprisingly low value (10% within a 4 km buffer); landscape metrics exert different effects on species occupancy and abundance in high versus low population density regions of our study area. We conclude that knowledge of regional variation in landscape utilization will be essential for successful conservation of the species. The results also support the view that large-scale landscape variables have high predictive power in explaining species abundance. Our study demonstrates the complex response of species occurrence at different levels of population configuration on landscape structure. The study also highlights the need for data in large spatial scale to increase the precision of biodiversity mapping and prediction of future trends.

Pulsed food resources, but not forest cover, determine lifetime reproductive success in a forest-dwelling rodent.

The relative contributions of habitat and food availability on fitness may provide evidence for key habitat features needed to safeguard population persistence. However, defining habitat quality for a species can be a complex task, especially if knowledge on the relationship between individual performance and habitat quality is lacking. Here, we determined the relative importance of the availability of suitable forest habitat, body mass and food from masting tree species on female lifetime reproductive success (LRS) of Siberian flying squirrels (Pteromys volans). We calculated LRS of 500 female flying squirrels based on a 22-year-long longitudinal dataset of two populations from western Finland. We assessed with generalised additive models the potential effects of availability of suitable habitat and cumulative lifetime availability of food from masting tree species on female LRS, longevity and fecundity. On a reduced dataset, we evaluated the importance of female winter body mass and conducted a piecewise path analysis to determine how variables were connected. According to generalised additive models female longevity, fecundity and LRS were mainly determined by variation in cumulative lifetime availability of food from masting alder and birch. Instead, habitat and body mass had a smaller role. The path analysis indicated that lifetime food availability had a direct effect on longevity and fecundity, and these had an equal effect on LRS at both study sites. Our results on LRS show that the occurrence of tree masting events during a female flying squirrel's lifetime has a profoundly larger effect on LRS than the cover of suitable forest habitat. Furthermore, this study emphasises the importance of both fecundity and longevity, and the indirect effects of food availability via those components, as determinants of lifetime fitness in female flying squirrels.

The evolution of site-selection strategy during dispersal.

We propose a mathematical model that enables the evolutionary analysis of site-selection process of dispersing individuals that encounter sites of high or low quality. Since each site can be inhabited by at most one individual, all dispersers are not able to obtain a high-quality site. We study the evolutionary dynamics of the low-quality-site acceptance as a function of the time during the dispersal season using adaptive dynamics. We show that environmental changes affect the evolutionary dynamics in two ways: directly and indirectly via density-dependent factors. Direct evolutionary effects usually follow intuition, whereas indirect effects are often counter-intuitive and hence difficult to predict without mechanistic modeling. Therefore, the mechanistic derivation of the fitness function, with careful attention on density- and frequency dependence, is essential for predicting the consequences of environmental changes to site selection. For example, increasing fecundity in high-quality sites makes them more tempting for dispersers and hence the direct effect of this ecological change delays the acceptance of low-quality sites. However, increasing fecundity in high-quality sites also increases the population size, which makes the competition for sites more severe and thus, as an indirect effect, forces evolution to favor less picky individuals. Our results indicate that the indirect effects often dominate the intuitive effects, which emphasizes the need for mechanistic models of the immigration process.

Role of breeding and natal movements in lifetime dispersal of a forest-dwelling rodent.

The lifetime movements of an individual determine the gene flow and invasion potential of the species. However, sex dependence of dispersal and selective pressures driving dispersal have gained much more attention than dispersal at different life and age stages. Natal dispersal is more common than dispersal between breeding attempts, but breeding dispersal may be promoted by resource availability and competition. Here, we utilize mark-recapture data on the nest-box population of Siberian flying squirrels to analyze lifetime dispersal patterns. Natal dispersal means the distance between the natal nest and the nest used the following year, whereas breeding movements refer to the nest site changes between breeding attempts. The movement distances observed here were comparable to distances reported earlier from radio-telemetry studies. Breeding movements did not contribute to lifetime dispersal distance and were not related to variation in food abundance or habitat patch size. Breeding movements of males were negatively, albeit not strongly, related to male population size. In females, breeding movement activity was low and was not related to previous breeding success or to competition between females for territories. Natal philopatry was linked to apparent death of a mother; that is, we did not find evidence for mothers bequeathing territories for offspring, like observed in some other rodent species. Our results give an example of a species in which breeding movements are not driven by environmental variability or nest site quality. Different evolutionary forces often operate in natal and breeding movements, and our study supports the view that juveniles are responsible for redistributing individuals within and between populations. This emphasizes the importance of knowledge on natal dispersal, if we want to understand consequences of movement ecology of the species at the population level.

Immigration ensures population survival in the Siberian flying squirrel.

Linking dispersal to population growth remains a challenging task and is a major knowledge gap, for example, for conservation management. We studied relative roles of different demographic rates behind population growth in Siberian flying squirrels in two nest-box breeding populations in western Finland. Adults and offspring were captured and individually identifiable. We constructed an integrated population model, which estimated all relevant annual demographic rates (birth, local [apparent] survival, and immigration) as well as population growth rates. One population (studied 2002-2014) fluctuated around a steady-state equilibrium, whereas the other (studied 1995-2014) showed a numerical decline. Immigration was the demographic rate which showed clear correlations to annual population growth rates in both populations. Population growth rate was density dependent in both populations. None of the demographic rates nor the population growth rate correlated across the two study populations, despite their proximity suggesting that factors regulating the dynamics are determined locally. We conclude that flying squirrels may persist in a network of uncoupled subpopulations, where movement between subpopulations is of critical importance. Our study supports the view that dispersal has the key role in population survival of a small forest rodent.

Siberian flying squirrels do not anticipate future resource abundance.

BACKGROUND: One way to cope with irregularly occurring resources is to adjust reproduction according to the anticipated future resource availability. In support of this hypothesis, few rodent species have been observed to produce, after the first litter born in spring, summer litters in anticipation of autumn's seed mast. This kind of behaviour could eliminate or decrease the lag in population density normally present in consumer dynamics. We focus on possible anticipation of future food availability in Siberian flying squirrels, Pteromys volans. We utilise long-term data set on flying squirrel reproduction spanning over 20 years with individuals living in nest-boxes in two study areas located in western Finland. In winter and early spring, flying squirrels depend on catkin mast of deciduous trees. Thus, the temporal availability of food resource for Siberian flying squirrels is similar to other mast-dependent rodent species in which anticipatory reproduction has been observed. RESULTS: We show that production of summer litters was not related to food levels in the following autumn and winter. Instead, food levels before reproduction, in the preceding winter and spring, were related to production of summer litters. In addition, the amount of precipitation in the preceding winter was found to be related to the production of summer litters. CONCLUSIONS: Our results support the conclusion that Siberian flying squirrels do not anticipate the mast. Instead, increased reproductive effort in female flying squirrels is an opportunistic event, seized if the resource situation allows.

Immediate or lagged responses of a red squirrel population to pulsed resources.

According to producer-consumer models, consumers should follow pulsed resources with a time lag. This view has been challenged by studies demonstrating that individuals may anticipate future resource pulses by increasing reproduction just before the pulse. We studied population fluctuations and reproduction in European red squirrels, Sciurus vulgaris, in relation to seed masting of the main food resource (the Norway spruce) in boreal coniferous forests between 1979 and 2013. Red squirrels are pre-dispersal seed predators, and previous studies have shown that they can anticipate the coming seed mast. We did not find any indication that anticipation of masting (year t ) increased red squirrel reproduction in the preceding spring to early summer. Instead, the reproductive output of the squirrels was highest in the spring following the mast, indicating that the population had to be at its largest size in the autumn after the mast (year(t+1)), when lots of subadults were around. However, we surmised, based on snow tracks and squirrel nest data, that the population crashed during the following winter (year(t+1)). These data reflected the adult population during winter, which peaked at the same time as the resource pulse. We can therefore conclude that the time lag between the resource pulse and the attainment of the peak number of squirrels was less than one year, and that the resource crash affected more juveniles and subadults than adults. The population increase overlapped with the occurrence of masting, but there was also a lagged response, supporting the classical view of producer-consumer models.

Condition-dependent, phenotype-dependent and genetic-dependent factors in the natal dispersal of a solitary rodent.

1. Dispersal can be condition- and phenotype-dependent and related to individual genetic differences. Few studies have addressed the relative importance of these factors on dispersal. We studied the factors behind philopatry and dispersal in juvenile Siberian flying squirrels, Pteromys volans L. 2. The dispersal distance and the distances explored before abandoning the natal nest were not related to any of the condition-dependent factors studied such as the area of high-quality habitat or the number of conspecifics near the natal area. In addition, the body mass (a phenotypic trait) of individuals was not related to philopatry and dispersal in flying squirrels. 3. Genetic variability, measured by microsatellite heterozygosity, was positively correlated with dispersal. The correlation was mainly driven by one locus related to the distances explored before abandoning the natal nest. 4. We conclude that condition- and phenotype-dependent factors did not have detectable effects on philopatry and dispersal, but individual heterozygosity was related to dispersal in flying squirrels. Our results suggest that genetic variability is important behind the dispersal of the species.

Natal habitat-biased dispersal in the Siberian flying squirrel.

Theoretically, dispersers should target the habitat where prospects for fitness will be highest. Aiming for a habitat similar to the natal area (natal habitat-biased dispersal) has been hypothesized as a probable rule of thumb for dispersers, but has received very little empirical support to date. We investigated similarities between natal and post-dispersal settlement sites with radio-collared Siberian flying squirrels (Pteromys volans L.). Juveniles born in small patches and raised in nests close to patch edge settled in small patches and used nests close to edges after dispersal. In addition, post-dispersal use of dreys (versus cavities) was similar to that observed in natal sites. However, the quality of settlement habitat was unrelated to the quality of the natal site, which suggests that natal experience on average-quality habitats may not lead to ecological traps for flying squirrels. This study provides evidence that habitat selection at the landscape scale is influenced by habitat of natal area.

Habitat exploration and use in dispersing juvenile flying squirrels.

1. Variation in behaviours involved in habitat selection is important for several evolutionary and ecological processes. For example, habitat use during dispersal may differ from breeding habitat use, and for dispersers the scale of habitat familiarity is determined by exploratory behaviour. We studied habitat use and exploration of 56 radio-collared juvenile flying squirrels Pteromys volans L. within natal home range and during dispersal, and compared habitat use between juveniles and 37 adults within breeding home range. 2. Before dispersal, young flying squirrels actively moved around the natal site. Surprisingly, long-distance dispersers explored less than short-distance dispersers, but philopatric individuals explored similar distances as dispersers. Females explored less than males, although females are the more dispersive sex in flying squirrels. 3. For most of the individuals the settlement area was unfamiliar due to long dispersal distance. Consequently, direction and distance of exploration were not very strong predictors of settlement location. However, individuals familiar with the settlement area concentrated exploration to that area. Exploration did not correlate with short-term survival. 4. Dispersers preferred breeding habitat while dispersing, but were found more often in matrix habitat than juveniles within natal, or adults within breeding, home ranges. 5. We conclude that familiarity does not determine settlement as much as, for example, availability of the habitat for flying squirrels. Based on our results, it also seems clear that data on adult habitat use are not enough to predict habitat use of dispersing individuals. In addition, our results support the recent view that short- and long-distance dispersers may need to be analysed separately in ecological and evolutionary analyses.

Metapopulation structure and movements in five species of checkerspot butterflies.

We studied the patterns and rates of migration among habitat patches for five species of checkerspot butterflies (Lepidoptera: Melitaeini) in Finland: Euphydryas aurinia, E. maturna, Melitaea cinxia, M. diamina and M. athalia. We applied the virtual migration (VM) model to mark-release-recapture data collected from multiple populations. The model includes parameters describing migration and survival rates and how they depend on the areas and connectivities of habitat patches. The number of individuals captured varied from 73 to 1,123, depending on species and sex, and the daily recapture probabilities varied between 0.09-0.52. The VM model fitted the data quite well. The results show that the five species are broadly similar in their movement rates and patterns, though, e.g. E. maturna tends to move shorter distances than the other species. There is no indication of any phylogenetic component in the parameter values. The parameter values estimated for each species suggest that a large percentage (80-90%) of migration events were successful in the landscapes that were studied. The area of the habitat patch had a substantial effect on emigration and immigration rates, such that butterflies were more likely to leave small than large patches and large patches were more likely than small patches to receive immigrants.