Habitat requirements of deadwood-dependent invertebrates that occupy tree hollows.

Tree hollows support a specialised species-rich fauna. We review the habitat requirements of saproxylic (= deadwood dependent) invertebrates which occupy tree hollows. We focus on studies quantifying relationships between species occurrence patterns and characteristics of tree hollows, hollow trees, and the surrounding landscape. We also explore the processes influencing species occurrence patterns by reviewing studies on the spatio-temporal dynamics of populations, including their dispersal and genetic structure. Our literature search in the database Scopus identified 52 relevant publications, all of which were studies from Europe. The dominant taxonomic group studied was beetles. Invertebrates in hollow trees were often more likely to be recorded in trees with characteristics reflecting a large amount of resources or a stable and warm microclimate, such as a large diameter, large amounts of wood mould (= loose material accumulated in the hollows mainly consisting of decaying wood), a high level of sun exposure, and with entrance holes that are large and either at a low or high height, and in dry hollows, with entrances not directed upwards. A stable microclimate is probably a key factor why some species of saproxylic invertebrates are confined to tree hollows. Other factors that are different in comparison to downed dead wood is the fact that hollows at a given height from the ground provide shelter from ground-living predators, that hollows persist for longer, and that the content of nutrients might be enhanced by the accumulation of dead leaves, insect frass, and remains from dead insects. Several studies have identified a positive relationship between species occupancy per tree and the amount of habitat in the surrounding landscape, with a variation in the spatial scale at which characteristics of the surrounding landscape had the strongest effect over spatial scales from 200 to 3000 m. We found empirical support for the extinction threshold hypothesis, which predicts that the frequency of species presence per tree is greater if a certain number of trees are aggregated into a few large clusters of hollow trees rather than distributed among many small clusters. Observed thresholds in species occurrence patterns can be explained by colonisation-extinction dynamics, with species occupancy per tree influenced by variation in rates of immigration. Consistent with this assumption, field studies suggest that dispersal rate and range can be low for invertebrates occupying tree hollows, although higher in a warmer climate. For one species in which population dynamics has been studied over 25 years (Osmoderma eremita), the observed population dynamics have characteristics of a "habitat-tracking metapopulation", as local extinctions from trees occur possibly because those trees become unsuitable as well as due to stochastic processes in small populations. The persistence of invertebrate fauna confined to tree hollows may be improved by prolonging the standing life of existing hollow trees. It is also important to recruit new generations of hollow trees, preferably close to existing larger groups of hollow trees. Thus, the spatio-temporal dynamics of hollow trees is crucial for the invertebrate fauna that rely upon them.

Diversity of forest structures important for biodiversity is determined by the combined effects of productivity, stand age, and management.

In forests, the amount and diversity of structural features with high value for biodiversity, such as large trees and dead wood, are affected by productivity, stand age, and forest management. For efficient conservation of forest biodiversity, it is essential to understand the combined effects of these drivers. We used data from the Swedish National Forest Inventory to study the combined effects of productivity, stand age, and management for wood production on structures with high value for biodiversity: tree species richness, large living trees, dead wood volume, and specific dead wood types. Forest management changed the relationship between productivity and amount or diversity of some of the structures. Most structures increased with productivity and stand age, but decreased due to management. The negative effect of management was greatest for structures occurring mainly in high-productivity forests, such as deciduous dead wood. Thus, biodiversity conservation should target high-productivity forests to preserve these structures.

"Land-sparing benefits biodiversity while land-sharing benefits ecosystem services": Stakeholders' perspectives on biodiversity conservation strategies in boreal forests.

Biodiversity conservation and economic profit from forests can be combined by various land-sparing and land-sharing approaches. Using a semi-structured survey, we evaluated support for scenarios representing contrasting conservation strategies in a managed boreal forest landscape. Land-sparing approaches were supported by the conservation organisation, regional administrations and the forest company, mainly motivated by the benefit for biodiversity based on ecological theory. Land-sharing approaches were supported by one recreational organisation, some municipalities and the forest owners' association, mainly motivated by the delivery of ecosystem services. Stakeholder groups using certain ecosystem services had motivations that we related to an anthropocentric mindset, while others focused more on species conservation, which can be related both to an anthropocentric or an ecocentric mindsets. Forest conservation planning should consider stakeholders' preferences to handle land-use conflicts. Since reaching consensus among multiple stakeholders seems unfeasible, a combination of land-sparing and land-sharing approaches is probably the best compromise.

Land sharing complements land sparing in the conservation of disturbance-dependent species.

Alteration of natural disturbances in human-modified landscapes has resulted in many disturbance-dependent species becoming rare. Conservation of such species requires efforts to maintain or recreate disturbance regimes. We compared benefits of confining efforts to habitats in protected areas (a form of land sparing) versus integrating them with general management of production land (a form of land sharing), using two examples: fire in forests and grazing in semi-natural grasslands. We reviewed empirical studies from the temperate northern hemisphere assessing effects of disturbances in protected and non-protected areas, and compiled information from organisations governing and implementing disturbances in Sweden. We found advantages with protection of areas related to temporal continuity and quality of disturbances, but the spatial extent of disturbances is higher on production land. This suggests that an approach where land sparing is complemented with land sharing will be most effective for preservation of disturbance-dependent species in forests and semi-natural grasslands.

Protected area designation and management in a world of climate change: A review of recommendations.

Climate change is challenging conservation strategies for protected areas. To summarise current guidance, we systematically compiled recommendations from reviews of scientific literature (74 reviews fitting inclusion criteria) about how to adapt conservation strategies in the face of climate change. We focussed on strategies for designation and management of protected areas in terrestrial landscapes, in boreal and temperate regions. Most recommendations belonged to one of five dominating categories: (i) Ensure sufficient connectivity; (ii) Protect climate refugia; (iii) Protect a few large rather than many small areas; (iv) Protect areas predicted to become important for biodiversity in the future; and (v) Complement permanently protected areas with temporary protection. The uncertainties and risks caused by climate change imply that additional conservation efforts are necessary to reach conservation goals. To protect biodiversity in the future, traditional biodiversity conservation strategies should be combined with strategies purposely developed in response to a warming climate.

Microclimatic conditions mediate the effect of deadwood and forest characteristics on a threatened beetle species, Tragosoma depsarium.

While climate change has increased the interest in the influence of microclimate on many organisms, species inhabiting deadwood have rarely been studied. Here, we explore how characteristics of forest stands and deadwood affect microclimate inside deadwood, and analyse how this affects wood-living organisms, exemplified by the red-listed beetle Tragosoma depsarium. Deadwood and forest variables explained much of the variation in temperature, but less of the variation in moisture within deadwood. Several variables known to influence habitat quality for deadwood-dependent species were found to correlate with microclimate. Standing deadwood and an open canopy generates warmer conditions in comparison to downed logs and a closed canopy, and shaded, downed and large-diameter wood have higher moisture and more stable daily temperatures than sun-exposed, standing, and small-diameter wood. T. depsarium occupancy and abundance increased with colder and more stable winter temperatures, and with higher spring temperatures. Consistently, the species occurred more frequently in deadwood items with characteristics associated with these conditions, i.e. downed large-diameter logs occurring in open conditions. Conclusively, microclimatic conditions were found to be important for a deadwood-dependent insect, and related to characteristics of both forest stands and deadwood items. Since microclimate is also affected by macroclimatic conditions, we expect species' habitat requirements to vary locally and regionally, and to change due to climate warming. Although many saproxylic species preferring sun-exposed conditions would benefit from a warmer climate per se, changes in species interactions and land use may still result in negative net effects of climate warming.

Increase in dead wood, large living trees and tree diversity, yet decrease in understory vegetation cover: The effect of three decades of biodiversity-oriented forest policy in Swedish forests.

In Sweden, the majority of forest area has been altered by industrial forestry over the decades. Almost 30 years ago, a shift towards biodiversity-oriented forest management practices occurred. Here we took advantage of long-term data collected by the Swedish National Forest Inventory to track developmental changes in forest structural components over this time. We assessed changes in structural components that play an important role in biodiversity (dead wood, large living trees, tree species composition, and understory vegetation) in four forest types with descending tiers of biodiversity protection: protected areas, woodland key habitats, low-productivity forests and production forests. Overall, we found a positive trend in the volumes of dead wood and large living trees, as well as in tree species diversity, while there was a general decline in understory vegetation coverage. Most observed changes were consistent with the intended outcomes of the current forest policy, adapted in the early 1990s. The implementation of retention forestry is likely driving some of the observed changes in forest structural components in the south. In contrast, we observed no changes in any of the focal structural components in the north, which could be attributed to the ongoing clear-cutting of forests previously managed less intensively. Dead wood and large living trees increased not only in managed, but also in unmanaged forests, likely reflecting historical management. The increased tree species diversity can be explained through current forest management practices that encourages maintenance of additional tree species. Decreasing understory vegetation coverage in both dense managed and unmanaged forests suggests that factors other than forestry contribute to the ongoing changes in understory vegetation in Swedish forests. Overall, the observed increase in structural components has not yet been reflected in documented improvements for red-listed forest species, which may be due to delays in species responses to small improvements, as well as a lack of detailed monitoring. Similarly, the increased availability of forest structural components might still be insufficient to meet the specific habitat requirements of red-listed species.

Operationalisation of ecological compensation - Obstacles and ways forward.

Ecological compensation (EC) has been proposed as an important tool for stopping the loss of biodiversity and natural values. However, there are few studies on its actual operationalisation and there is high uncertainty about how it should be designed and implemented to be an effective way of performing nature conservation. In this study we focus on ecological compensation in Sweden, a country where it is in the process of being implemented more broadly. Using interviews and a workshop we investigate how the work with the implementation is carried out and what challenges exist. The results show that implementation of EC is at an early stage of development and there are many practical obstacles, linked to both legislation and routines in the planning processes. There is a lack of holistic perspective and large-scale thinking, a quite strong focus on a small number of individual species, and an overall attitude that anything is better than nothing, all of which can have negative consequences for biodiversity conservation overall. Based on the results we discuss the need for better integration of EC into the entire decision-making process and for a holistic approach to preservation of biodiversity and ecosystem services, by increasing the focus on landscape perspective and considering delays in compensation outcomes. There is also a need for a national level standard for EC, making good and worse examples of compensation measures available and systematic monitoring of EC projects. Finally, a spatially explicit database to document all EC areas should be introduced both to ensure consistency in protection from future development plans and to enable long-term monitoring of EC outcomes.

Do different growth rates of trees cause distinct habitat qualities for saproxylic assemblages?

In production forests, a common silvicultural objective is enhancing tree growth rates. The growth rate influences both mechanical and biochemical properties of wood, which may have an impact on dead wood inhabiting (i.e. saproxylic) species. In this study, we tested for the first time whether tree growth rates affect dead-wood associated assemblages in general and the occurrence of red-listed species in particular. We sampled saproxylic beetles (eclector traps) and fungi (DNA metabarcoding of wood samples) in dead trunks of Norway spruce (Picea abies), which had different growth rates within the same hemiboreal forests in Sweden. A high proportion of fungi showed a positive association to increasing tree growth. This resulted in higher fungal richness in fast-grown trees both at the trunk scale and across multiple studied trunks. Such patterns were not observed for saproxylic beetles. However, a set of species (both beetles and fungi) preferred slow-grown wood. Moreover, the total number of red-listed species was highest in slow-grown trunks. We conclude that dead wood from slow-grown trees hosts relatively fewer saproxylic species, but a part of these may be vulnerable to production forestry. It implies that slow-grown trees should be a target in nature conservation. However, where slow-grown trees are absent, for instance in forests managed for a high biomass production, increasing the volumes of dead wood from fast-grown trees may support many species.

Increasing the amount of dead wood by creation of high stumps has limited value for lichen diversity.

Artificial creation of dead wood in managed forests can be used to mitigate the negative effects of forestry on biodiversity. For this to be successful, it is essential to understand the conservation value that the created dead wood has in comparison to naturally occurring dead wood, and, furthermore, where in the landscape addition of dead wood is most beneficial, i.e. how landscape composition influences species occurrence on dead wood. We examined these questions by surveying epixylic lichens on artificially created high stumps of Scots pine (Pinus sylvestris) in 3-17 years old clear-cuts. We compared lichen assemblages on high stumps to those on other types of pine dead wood in mature forests, and examined how stump age, the amount of dead wood at the clear-cuts, and landscape composition at 500 m - 2.5 km scale influenced the assemblages. In comparison to other dead wood types, high stumps hosted lower lichen richness and less variable assemblages containing mainly common generalist species. Species richness increased with stump age, whereas dead wood amount and landscape composition were not important; only the total amount of forests in the landscape had a minor positive effect. We conclude that at the studied timescale high stumps of Scots pine are not particularly valuable for epixylic lichens and provide a poor substitute for naturally occurring dead wood in mature forests, although their value may increase with age. Furthermore, directing dead wood creation to specific stands or landscapes does not appear beneficial for lichen biodiversity, given the minor effect of landscape composition found at scales below 2.5 km.

Metapopulation dynamics over 25 years of a beetle, Osmoderma eremita, inhabiting hollow oaks.

Osmoderma eremita is a species of beetle that inhabits hollows in ancient trees, which is a habitat that has decreased significantly during the last century. In southeastern Sweden, we studied the metapopulation dynamics of this beetle over a 25 year period, using capture-mark-recapture. The metapopulation size had been rather stable over time, but in most of the individual trees there had been a positive or negative trend in population development. The probability of colonisation was higher in well-connected trees with characteristics reflecting earlier successional stages, and the probability of extinction higher in trees with larger diameter (i.e. in later successional stages), which is expected from a habitat-tracking metapopulation. The annual tree mortality and fall rates (1.1% and 0.4%, respectively) are lower than the colonisation and extinction rates (5-7%), indicating that some of the metapopulation dynamics are due to the habitat dynamics, but many colonisations and extinctions take place for other reasons, such as stochastic events in small populations. The studied metapopulation occurs in an area with a high density of hollow oaks and where the oak pastures are still managed by grazing. In stands with fewer than ten suitable trees, the long-term extinction risk may be considerable, since only a small proportion of all hollow trees harbours large populations, and the population size in trees may change considerably during a decade.

Keeping pace with forestry: Multi-scale conservation in a changing production forest matrix.

The multi-scale approach to conserving forest biodiversity has been used in Sweden since the 1980s, a period defined by increased reserve area and conservation actions within production forests. However, two thousand forest-associated species remain on Sweden's red-list, and Sweden's 2020 goals for sustainable forests are not being met. We argue that ongoing changes in the production forest matrix require more consideration, and that multi-scale conservation must be adapted to, and integrated with, production forest development. To make this case, we summarize trends in habitat provision by Sweden's protected and production forests, and the variety of ways silviculture can affect biodiversity. We discuss how different forestry trajectories affect the type and extent of conservation approaches needed to secure biodiversity, and suggest leverage points for aiding the adoption of diversified silviculture. Sweden's long-term experience with multi-scale conservation and intensive forestry provides insights for other countries trying to conserve species within production landscapes.

Correction to: Keeping pace with forestry: Multi-scale conservation in a changing production forest matrix.

In the original published article, the sentence "Nevertheless, semi-natural forest remnants continue to be harvested and fragmented (Svensson et al. 2018; Jonsson et al. 2019), and over 2000 forest-associated species (of 15 000 assessed) are listed as threatened on Sweden's red-list, largely represented by macro-fungi, beetles, lichens and butterflies (Sandström 2015)."under the section Introduction was incorrect. The correct version of the sentence is "Nevertheless, semi-natural forest remnants continue to be harvested and fragmented (Svensson et al. 2018; Jonsson et al. 2019), and approximately 2000 forest-associated species (of 15 000 assessed) are on Sweden's red-list, largely represented by macro-fungi, beetles, lichens and butterflies (Sandström 2015)."

The evolutionary species pool concept does not explain occurrence patterns of dead-wood-dependent organisms: implications for logging residue extraction.

Emulation of natural disturbances is often regarded as a key measure to make forestry biodiversity-oriented. Consequently, extraction of logging residues is assumed to have little negative effect in comparison to extraction of dead wood mainly formed at natural disturbances. This is consistent with the evolutionary species pool hypothesis, which suggests that most species are evolutionary adapted to the naturally most abundant habitats. We tested this hypothesis for dead-wood-dependent macrofungi, lichens, and beetles in a boreal forest landscape in central Sweden, assuming that species are adapted to conditions similar to today's unmanaged forest. No occurrence patterns, for the species groups which we investigated, were consistent with the hypothesis. Overall, stumps and snags had the highest habitat quality (measured as average population density with equal weight given to each species) and fine woody debris the lowest, which was unexpected, since stumps were the rarest dead-wood type in unmanaged forest. We conclude that the evolutionary species pool concept did not explain patterns of species' occurrences, and for two reasons, the concept is not reliable as a general rule of thumb: (1) what constitute habitats harbouring different species communities can only be understood from habitat-specific studies and (2) the suitability of habitats is affected by their biophysical characteristics. Thus, emulation of natural disturbances may promote biodiversity, but empirical studies are needed for each habitat to understand how natural disturbances should be emulated. We also conclude that stump extraction for bioenergy is associated with larger risks for biodiversity than fine woody debris extraction.

Abundance-based detectability in a spatially-explicit metapopulation: a case study on a vulnerable beetle species in hollow trees.

In many fragmented habitats, the detectability of a population in a habitat patch closely depends on the local abundance of individuals. However, metapopulation studies rarely connect abundance and detectability. We propose a framework for using abundance-based estimates of detectability in the analysis of a spatially-explicit stochastic patch occupancy model (SPOM). We illustrate our approach with the example of Tenebrio opacus, a beetle inhabiting hollows in old trees, and have based it on a 6-year monitoring programme of adult beetles in an area harbouring a high density of old oaks. We validated our abundance-based methodology by showing that the estimates of detectability were positively and significantly correlated with those obtained from presence/absence data (Pearson r = 0.54, p < 2E-16) in our study system. We further showed that the height of the hollow on the tree and the area of its entrance hole, the living status and girth of the host tree, and the time of survey significantly affected the detectability of beetle populations. Median detectability was 51% for one survey. The SPOM analysis revealed a high but heterogeneous extinction risk among trees, suggesting a metapopulation dynamics between the "classic" and "mainland-island" paradigms. However, it also indicated unexplained beetle colonization of trees in our study, despite the fact that we included limited detectability in our estimation procedure. This may have been due to the cryptic larval stage of T. opacus and may thus invalidate the use of a classic SPOM in our study system.

Conservation value of low-productivity forests measured as the amount and diversity of dead wood and saproxylic beetles.

In many managed landscapes, low-productivity land comprises most of the remaining relatively untouched areas, and is often over-represented within protected areas. The relationship between the productivity and conservational value of a site is poorly known; however, it has been hypothesized that biodiversity increases with productivity due to higher resource abundance or heterogeneity, and that the species communities of low-productivity land are a nested subset of communities from more productive land. We tested these hypotheses for dead-wood-dependent beetles by comparing their species richness and composition, as well as the amount and diversity of dead wood, between low-productivity (potential forest growth <1 m3 ·ha-1 ·yr-1 ) and high-productivity Scots pine-dominated stands in Sweden. We included four stand types: stands situated on (1) thin soils and (2) mires (both low-productivity), (3) managed stands, and (4) unmanaged stands set aside for conservation purposes (both high-productivity). Beetle species richness and number of red-listed species were highest in the high-productivity set-asides. Species richness was positively correlated with the volume and diversity of dead wood, but volume appeared to be a better predictor than diversity for the higher species richness in set-asides. Beetle species composition was similar among stand types, and the assemblages in low-productivity stands were largely subsets of those in high-productivity set-asides. However, 11% of all species and 40% of red-listed species only occurred in high-productivity stands, while no species were unique to low-productivity stands. We conclude that low-productivity forests are less valuable for conservation than high-productivity forest land. Given the generally similar species composition among stand types, a comparable conservational effect could be obtained by setting aside a larger area of low-productivity forest in comparison to the high-productivity. In terms of dead wood volumes, 1.8-3.6 ha of low-productivity forest has the same value as 1 ha of unmanaged high-productivity forest. This figure can be used to estimate the conservation value of low-productivity forests; however, as high-productivity forests harbored some unique species, they are not completely exchangeable.

The effects of logging residue extraction for energy on ecosystem services and biodiversity: A synthesis.

We review the consequences for biodiversity and ecosystem services from the industrial-scale extraction of logging residues (tops, branches and stumps from harvested trees and small-diameter trees from thinnings) in managed forests. Logging residue extraction can replace fossil fuels, and thus contribute to climate change mitigation. The additional biomass and nutrients removed, and soils and other structures disturbed, have several potential environmental impacts. To evaluate potential impacts on ecosystem services and biodiversity we reviewed 279 scientific papers that compared logging residue extraction with non-extraction, the majority of which were conducted in Northern Europe and North America. The weight of available evidence indicates that logging residue extraction can have significant negative effects on biodiversity, especially for species naturally adapted to sun-exposed conditions and the large amounts of dead wood that are created by large-scaled forest disturbances. Slash extraction may also pose risks for future biomass production itself, due to the associated loss of nutrients. For water quality, reindeer herding, mammalian game species, berries, and natural heritage the results were complicated by primarily negative but some positive effects, while for recreation and pest control positive effects were more consistent. Further, there are initial negative effects on carbon storage, but these effects are transient and carbon stocks are mostly restored over decadal time perspectives. We summarize ways of decreasing some of the negative effects of logging residue extraction on specific ecosystem services, by changing the categories of residue extracted, and site or forest type targeted for extraction. However, we found that suggested pathways for minimizing adverse outcomes were often in conflict among the ecosystem services assessed. Compensatory measures for logging residue extraction may also be used (e.g. ash recycling, liming, fertilization), though these may also be associated with adverse environmental impacts.

Modified forest rotation lengths: Long-term effects on landscape-scale habitat availability for specialized species.

We evaluated the long-term implications from modifying rotation lengths in production forests for four forest-reliant species with different habitat requirements. By combining simulations of forest development with habitat models, and accounting both for stand and landscape scale influences, we projected habitat availability over 150 years in a large Swedish landscape, using rotation lengths which are longer (+22% and +50%) and shorter (-22%) compared to current practices. In terms of mean habitat availability through time, species requiring older forest were affected positively by extended rotations, and negatively by shortened rotations. For example, the mean habitat area for the treecreeper Certhia familiaris (a bird preferring forest with larger trees) increased by 31% when rotations were increased by 22%, at a 5% cost to net present value (NPV) and a 7% decrease in harvested volume. Extending rotation lengths by 50% provided more habitat for this species compared to a 22% extension, but at a much higher marginal cost. In contrast, the beetle Hadreule elongatula, which is dependent on sun-exposed dead wood, benefited from shortened rather than prolonged rotations. Due to an uneven distribution of stand-ages within the landscape, the relative amounts of habitat provided by different rotation length scenarios for a given species were not always consistent through time during the simulation period. If implemented as a conservation measure, prolonging rotations will require long-term strategic planning to avoid future bottlenecks in habitat availability, and will need to be accompanied by complementary measures accounting for the diversity of habitats necessary for the conservation of forest biodiversity.

Temperature drives abundance fluctuations, but spatial dynamics is constrained by landscape configuration: Implications for climate-driven range shift in a butterfly.

Prediction of species distributions in an altered climate requires knowledge on how global- and local-scale factors interact to limit their current distributions. Such knowledge can be gained through studies of spatial population dynamics at climatic range margins. Here, using a butterfly (Pyrgus armoricanus) as model species, we first predicted based on species distribution modelling that its climatically suitable habitats currently extend north of its realized range. Projecting the model into scenarios of future climate, we showed that the distribution of climatically suitable habitats may shift northward by an additional 400 km in the future. Second, we used a 13-year monitoring dataset including the majority of all habitat patches at the species northern range margin to assess the synergetic impact of temperature fluctuations and spatial distribution of habitat, microclimatic conditions and habitat quality, on abundance and colonization-extinction dynamics. The fluctuation in abundance between years was almost entirely determined by the variation in temperature during the species larval development. In contrast, colonization and extinction dynamics were better explained by patch area, between-patch connectivity and host plant density. This suggests that the response of the species to future climate change may be limited by future land use and how its host plants respond to climate change. It is, thus, probable that dispersal limitation will prevent P. armoricanus from reaching its potential future distribution. We argue that models of range dynamics should consider the factors influencing metapopulation dynamics, especially at the range edges, and not only broad-scale climate. It includes factors acting at the scale of habitat patches such as habitat quality and microclimate and landscape-scale factors such as the spatial configuration of potentially suitable patches. Knowledge of population dynamics under various environmental conditions, and the incorporation of realistic scenarios of future land use, appears essential to provide predictions useful for actions mitigating the negative effects of climate change.