Large-scale population dynamics of the Eurasian red squirrel

The size of an animal population is determined by the birth rate, mortality, and movement of individuals between populations. These demographic parameters, in turn, are affected by internal and external factors. Internal factors include, for example, the density and the sex ratio of the focal population. External factors can be divided to biotic and abiotic factors. In this thesis, I study the population dynamics of the Eurasian red squirrel (Sciurus vulgaris) and factors affecting it on different scales by utilizing snowtrack data, old hunting data and data on nest box occupancy. The red squirrel is widely distributed and common in boreal coniferous forests, and it acts both as a seed disperser and as an alternative prey for several predator species at the low phases of the vole cycle. It has also been an important game mammal, and red squirrel hunting was popular in Finland until the mid-1900s. The results of my thesis show that red squirrel populations fluctuate synchronously within hundreds of kilometers, and that this synchrony is driven by similarly fluctuating and spatially autocorrelated spruce (Picea abies) cone crop. The main predators, the pine marten (Martes martes) and the goshawk (Accipiter gentilis), on the other hand, do not negatively affect red squirrel numbers on the population level. On a smaller scale, however, both the red squirrel and the flying squirrel (Pteromys volans) more likely occupied nest boxes that were far from the nests of avian predators. Thus, the squirrels and their predators are negatively associated on individual level, but the red squirrel and its predators are positively associated on a larger scale. The variation in red squirrel numbers between census sites and years was most strongly affected by spruce cone crop. However, cone crop did not explain the remarkable variations in the red squirrel sex ratio, which were demonstrated by the re-analysis of old hunting data. Overall, food availability emerges as the most significant determinant of red squirrel population density, exceeding the direct and indirect effects of predators. I also found out that the red squirrel is well adapted to human-altered landscape and may even favor mosaic-like areas, even though it is arboreal and adapted to a life in the forest canopy. Both the snow-track data and nest box data suggest that there are more red squirrels near human settlement and in agricultural areas than in continuous forests. A mosaic-like landscape provides red squirrels with alternative food resources, which makes them less dependent on the highly variable conifer cone crop. The apparent preference for agricultural areas by both the red squirrel and the flying squirrel may be partially explained by the higher productivity of forest edges. Even though a red squirrel is still a common sight in backyards and bird-feeding sites, it seems that the species has declined in forests. The analysis of the snow-track data from Finland and north-western Russia revealed that the red squirrel declined in most parts of the 1000000 km2-study area between 1996 and 2012. This alarming trend is partially due to the global warming. I found that the red squirrel population growth rate was lowest in those regions where winters warmed the most. Other climatic parameters, deforestation, and the simultaneous increase in pine marten populations did not explain the decline of the red squirrel. The exact mechanism of how winter warming is detrimental for the red squirrel calls for further studies. The Finnish snow-track data from 1989 to 2017 shows that the red squirrel increased in Southern Finland but declined in other parts of the country. Drawn together, the results of this thesis show that synchrony occurs between red squirrel populations on a scale of hundreds of kilometers, and that the large-scale population dynamics are driven by conifer seed crop while predators have only a minor role. The red squirrel has adapted well to many anthropogenic changes, such as built areas and agricultural fields fragmenting forests, but the global warming seems to pose a threat to it. Studying the changes in red squirrel populations can help understand ecosystems of the boreal forests and the way anthropogenic changes affect them.Eläinpopulaation sisäiset ja ulkoiset tekijät vaikuttavat populaatiokokoon syntyvyyden, kuolleisuuden ja muuttoliikkeen kautta. Sisäisiä eli populaatioon itseensä liittyviä tekijöitä ovat esimerkiksi sukupuolijakauma ja tiheys. Ulkoiset tekijät puolestaan voidaan jakaa eliöiden välisiin vuorovaikutuksiin ja ympäristötekijöihin. Tässä väitöskirjassa tarkastelen oravan (Sciurus vulgaris) populaatiodynamiikkaa ja siihen vaikuttavia tekijöitä eri mittakaavoissa lumijälkiaineistojen, vanhojen metsästysaineistojen ja pönttöjen asutusaineistojen perusteella. Orava on yleinen ja laajalle levinnyt pohjoisella havumetsävyöhykkeellä, ja sillä on tärkeä rooli ekosysteemissä puiden siementen levittäjänä ja monien petojen vaihtoehtoisena saalislajina myyräkantojen ollessa alhaalla. Se on ollut myös tärkeä riistaeläin Suomessa aina 1900-luvun puoliväliin saakka. Tutkimuksissani selvisi, että oravapopulaatioiden koko vaihtelee samanaikaisesti ja -suuntaisesti satojen kilometrien laajuisilla alueilla, ja että tämän synkronisen vaihtelun syy on samalla tavalla voimakkaasti tilassa autokorreloitunut kuusen (Picea abies) käpysato. Oravan luontaisilla pääpedoilla, eli näädällä (Martes martes) ja kanahaukalla (Accipiter gentilis), ei puolestaan havaittu negatiivista vaikutusta oravamääriin populaatiotasolla. Pienemmässä mittakaavassa tarkasteltuna orava, ja myös liito-orava (Pteromys volans), kuitenkin käyttivät eniten sellaisia pönttöjä, jotka sijaitsivat kaukana petolintujen pesistä. Yksilötasolla oravat siis välttivät petoja, kun taas laajemmassa mittakaavassa orava ja sen saalistajat esiintyivät runsaina samoilla alueilla. Käpysato vaikutti myös voimakkaasti oravan runsauden vaihteluun eri laskenta-alueiden ja vuosien välillä. Käpysato ei kuitenkaan ollut yhteydessä oravan sukupuolijakaumaan, joka vaihteli laajoilla alueilla vanhan metsästysaineiston uudelleenanalysoinnin perusteella. Joka tapauksessa lajien välisistä vuorovaikutuksista ravinnon saatavuus ja sen vaihtelu olivat tärkeämpiä tekijöitä oravakantojen säätelyssä kuin petojen aiheuttama kuolleisuus tai petojen läsnäolon epäsuorat vaikutukset. Lisäksi, vaikka orava on sopeutunut elämään puissa ja on selkeästi metsälaji, se vaikuttaa sietävän hyvin ja jopa hyötyvän ihmisen muokkaamasta ympäristöstä. Oravia havaittiin enemmän lähellä ihmisasutusta ja maatalousympäristöä sekä lumijälki- että pönttöaineistoissa. Mosaiikkimainen, monipuolinen ympäristö tarjoaa oraville vaihtoehtoisia ravintoresursseja, jolloin ne eivät ole yhtä riipuvaisia voimakkasti vaihtelevasta kuusen käpysadosta kuin yhtenäisillä metsäalueilla. Valoisat, peltojen rajaamat metsänreunat saattavat olla muuta metsää tuottoisampia alueita, mikä selittäisi näennäisen avoimien alueiden suosimisen sekä oravalla että liito-oravalla. Vaikka oravat ovat yleinen näky ihmisten pihapiireissä, ne vaikuttavat vähentyneen metsissä. Suomen ja Luoteis-Venäjän lumijälkiaineistoista paljastui, että oravakannat laskivat suurimmassa osassa lähes miljoonan neliökilometrin tutkimusaluetta vuosien 1996–2012 välillä. Osasyy tähän huolestuttavaan kehitykseen vaikutti olevan ilmastonmuutos. Havaitsin, että oravan populaation kasvukerroin oli pienin niillä alueilla, joissa talvet lämpenivät eniten. Muut tarkastellut ilmastomuuttujat, metsien hakkuut ja näädän samanaikainen runsastuminen eivät olleet yhteydessä oravakannan laskuun. Ilmastonmuutoksen tarkka vaikutusmekanismi vaatii lisää tutkimuksia. Suomen lumijälkiaineiston perusteella orava runsastui Etelä-Suomessa vuosien 1989– 2017 välillä, mutta kanta on ollut laskussa muissa osissa maata. Väitöskirjani tulokset osoittavat, että oravien määrä vaihtelee synkronisesti satojen kilometrien laajuisilla alueilla, ja että laajan mittakaavan populaatiodynamiikka on vahvasti riippuvainen havupuiden siemensadosta, kun taas petojen rooli on verraten vähäinen. Orava on sopeutunut moniin ihmisen aiheuttamiin muutoksiin, kuten maatalouden pirstomaan maisemaan ja asutuksen läheisyyteen, mutta ilmastonmuutos saattaa vaikuttaa oraviin haitallisesti. Oravan kannanvaihtelujen tutkiminen auttaa osaltaan ymmärtämään pohjoisten havumetsien ekosysteemien toimintaa ja ihmisen vaikutuksia niissä sekä ilmaston että maisemarakenteen muutosten kautta

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

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.</p

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.Peer reviewe

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

Data from: 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

Nest-box occupancy data for flying squirrels

Data describes occupancy (1=precence, 0=absence) of flying squirrels in nest boxes. BCODE= name of nest box. ID = a unique combination of box name and census year. Ural owl and goshawk columns describe modelled predation risk from these predators at the nest box site, see article for methods. h1...h27 refer to different land use classes and their combinations as in Table 1 of the research article. _200m and _1km means area (square meters) of that habitat within 200 meters and 1km from nest box, respectively. s (for example h17_200ms) refers to standarized amount of that habitat, see methods

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

<div><p>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 (<i>Strix uralensis</i>) decreased occurrence of night-active flying squirrels (<i>Pteromys volans</i>) and diurnal goshawks (<i>Accipiter gentilis</i>) that of day-active red squirrels (<i>Sciurus vulgaris</i>). 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.</p></div