Edited by: Alberto Santini, Italian National Research Council, Italy
Reviewed by: Rose Marie Muzika, Carnegie Museum of Natural History, United States; Jürgen Bauhus, University of Freiburg, Germany
This article was submitted to Forest Disturbance, a section of the journal Frontiers in Forests and Global Change
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Invasive pathogens threaten the ability of forests globally to produce a range of valuable ecosystem services over time. However, the ability to detect such pathogen invasions—and thus to produce appropriate and timely management responses—is relatively low. We argue that a promising approach is to plan and manage forests in a way that increases their resilience to invasive pathogens not yet present or ubiquitous in the forest. This paper is based on a systematic search and critical review of empirical evidence of the effect of a wide range of forest management options on the primary and secondary infection rates of forest pathogens, and on subsequent forest recovery. Our goals are to inform forest management decision making to increase forest resilience, and to identify the most important evidence gaps for future research. The management options for which there is the strongest evidence that they increase forest resilience to pathogens are: reduced forest connectivity, removal or treatment of inoculum sources such as cut stumps, reduced tree density, removal of diseased trees and increased tree species diversity. In all cases the effect of these options on infection dynamics differs greatly amongst tree and pathogen species and between forest environments. However, the lack of consistent effects of silvicultural systems or of thinning, pruning or coppicing treatments is notable. There is also a lack of evidence of how the effects of treatments are influenced by the scale at which they are applied, e.g., the mixture of tree species. An overall conclusion is that forest managers often need to trade-off increased resilience to tree pathogens against other benefits obtained from forests.
Invasive species present significant threats to natural and planted forests (Wingfield et al.,
Managing invasive pathogens presents unique challenges not associated with controlling invasive plants and animals, including insects. The cryptic nature of infection by pathogens, particularly at the beginning of their life cycles, means that many invasions remain undetected until trees become symptomatic, by which time the pathogen is often already widespread (Liebhold et al.,
Tree pathogens threaten the ability of forests to deliver ecosystem services over the long-term. The importance of phytosanitary measures, such as quarantine, to reduce the risk of invasive tree pathogens reaching a country or a given forest have long been recognized (Wingfield et al.,
To help address this challenge, a recent extension of epidemiological modeling (“epi-economic modeling”) has linked the economics of forest management practices to the impacts of tree pathogens across a range of primary and secondary infection rates and damage costs (Macpherson et al.,
with
The fundamental difference between primary and secondary infection is epidemiological. Primary infection is the invasion of the population of trees within the forest management or landscape-patch unit from an external source, e.g., an infected population of trees in another unit, and requires management at the boundary or beyond. Primary infections can also occur from a reservoir of inoculum in alternative hosts, or in soil or dead plant material when sites are replanted. Thus, the source is “external” to the population under threat albeit occupying the same parcel of land. Secondary infection is transmission from currently infected trees within the unit's population to its susceptible trees, driven by multiplication, dispersal, and infection of inoculum. Hence management activity in that forest unit can influence secondary infection and reduce epidemic spread. The rates of primary and secondary infections in Equation (1) capture the whole range of factors, including the susceptibility of individual trees to infection as well as the dispersal characteristics of the pathogen.
Fundamental to this paper is the recognition that resilience of a forest is linked to its response to invasions by forest pathogens. This response, in turn, is influenced by the management practices aimed at the prevention of such invasions, their control and, if control is unsuccessful, the mitigation of their effects. The modeling framework described above and its extensions, have successfully been used in describing spread and control of tree pathogens in forests (Macpherson et al.,
The key question in ecological and economic applications of the concept of resilience is “resilience of what, to what?” (Walker et al.,
The impacts of forest management on tree pathogens have been the subject of many recent reviews. Each has tended to focus on a single pathogen, such as white pine blister rust (
The objective of the current study is to synthesize the evidence for the effect of forest management options on forest resilience to tree pathogens. The scope is broad, including all of the main categories of forest management variables and all tree pathogen species. However, animal pests, invasive plants and abiotic threats such as fire were excluded. A second objective is to forge an explicit link between forest resilience, forest design, or silvicultural management practices and epi-economic modeling grounded in plant and tree epidemiology (Macpherson et al.,
We carried out a literature review using a systematic search method to identify published sources of empirical data on the relationship between forest management and resilience to tree pathogens. We conducted an initial search of the peer-reviewed literature through Web of Science, using search strings to identify papers on all of forest management, pests, pathogens or disease, and resilience, excluding medical papers and those concerned with food supply, using the Boolean search string of:
TS = ((((*forest* OR wood* OR tree*) AND (manage*)) OR silvicult*) AND (pest* OR disease* OR pathogen*) AND (exposure OR resist* OR recover* OR spread OR risk OR suscept* OR transmit* OR dispers* OR infect*) NOT (medicin* OR clinic* OR pharma* OR foodborne OR food-borne OR mycorrhizal OR biomedic* OR mosquito OR tick OR lyme* OR malaria*)) NOT SO = (medicin* OR clinic* OR pharma* OR biomedic*) NOT WC = (medicin* OR clinic* OR pharma* OR biomedic*)
This search (run on 27/06/2017) returned 3,534 papers. The papers were screened first by title, then abstract, and finally full text to identify papers reporting original empirical data on the effects of forest management on tree diseases caused by pests or pathogens, which retained 599 papers. We then excluded papers that only covered tree pests (362 papers), were only concerned with tropical forests (85 papers) or orchards (235 papers), were concerned with tree breeding (74 papers), or were entirely review (23 papers) or theoretical modeling (21 papers) studies (note papers may be present in more than one category). Removal of tree pests also included removing papers concerning insect vectors, because in the majority of cases the distinction between direct damage and vectoring of a pathogen could not be determined. This procedure retained 81 papers. As many forest management actions are not reported in the published literature, searches were also run in TREESEARCH, the research portal for the US Forest Service, using the following search string:
(disease OR fung* OR pathogen OR bacteri* OR oomycete OR virus) AND (((tree OR forest* OR wood) AND manage*) OR silvicult*)
and the UK Forestry Commission website, using the search string:
disease fung* pathogen bacteria* oomycete virus
Restrictions on the search terms for each search engine prevented identical searches from being carried out. The search in TREESEARCH returned 158 documents, of which 12 were identified as relevant and containing data. The Forestry Commission website returned 58 documents, of which three were identified as relevant and containing data. Together with literature identified from the reference lists of retained papers and identified reviews (nine papers), and further search terms added to account for fertilizer application (four papers), the final reference list contained 114 papers and reports. This list was further refined to include only papers whose reliability, robustness and applicability to forest management could be assured. Studies which were purely descriptive, lab-based or considered only pathogen presence, rather than impact, were excluded. The remaining 109 papers included within the review were scored for strength of evidence based on whether they were correlative or experimental, and whether single or multiple sites had been considered, within single or multiple forests.
We organized papers by management technique, treating each technique reported within a single paper independently, and then by pathogen type. We have included a broad range of management options, including forest design planning, site preparation for forest establishment, tree species diversity, silvicultural system and individual silvicultural actions. These categories were not pre-determined but were decided through reading the papers.
To assess the outcome of each management technique we classified the results of each study as strong positive or strong negative (relationship observed in all sites within the study), weak positive or weak negative (relationship observed in at least one site within the study, with no sites showing the opposite relationship), no relationship, or mixed (both positive and negative relationships observed across sites). A technique was therefore considered to have an overall positive or negative impact where multiple studies, or a robust single study across multiple forests, found the same result, and there were no robust studies reporting a contradictory result. If studies reported contradicting results, we considered the outcome of this technique to be mixed unless the results were weighted heavily in one direction, and the contradicting study was considered to be of low robustness. Where only a limited number of studies was available this was identified as a weakness in our conclusions. A fuller description of this critical appraisal of the studies is provided in the
Overview of coverage of identified papers.
Location | |
North America (excluding California and Oregon coastal forests) | 35 |
California and Oregon coastal forests | 24 |
Europe | 29 |
Other | 11 |
Tree type | |
Broadleaf | 48 |
Conifer | 52 |
Pathogen type | |
Fungi (excluding Armillaria) | 48 |
Armillaria | 17 |
Oomycete (all phytophthora) | 21 |
General | 14 |
The large variation in tree species, pathogens, and management techniques considered, as well as limited reporting of the particulars of management, prevented us from conducting a formal meta-analysis.
Our review of the literature revealed a clear bias toward a small number of highly damaging pathogens. Studies into
A geographical bias was also evident, with 59% of studies based in North America, and California and Oregon coastal forests alone accounting for 24%. The majority of the remaining papers originate from Europe (29%), with eight papers from Oceania and two from Asia. Studies reporting only from natural tropical forests had previously been excluded. Only a single paper (Cleary et al.,
The response variables most commonly reported were mortality, disease incidence, and disease severity. The only indicator of forest recovery (defined in the section Introduction) that was widely reported was of subsequent tree growth rate, though this was often only measured over the short-term. There was minimal reporting of rates of tree natural regeneration. Studies generally reported outcomes in terms of symptoms of forest disease, and few papers considered the mechanisms connecting forest management to these outcomes. The distribution of studies amongst each forest management variable and each response variable is summarized in
Overview of published evidence of effects of forest management on resilience to tree diseases.
Connectivity | Mortality | Increased | Jules et al., |
Disease incidence | Increased | Hessburg, |
|
Disease severity | Increased | Condeso and Meentemeyer, |
|
Recovery | No data | ||
Previous land use | Mortality | No data | |
Disease incidence | Varied | Puddu et al., |
|
Disease severity | Increased in previous forest land | Meentemeyer et al., |
|
Recovery | No data | ||
Site preparation | Mortality | Decreased | Morrison et al., |
Disease incidence | Varied | Morrison et al., |
|
Disease severity | Varied | Blodgett et al., |
|
Recovery | Varied | Thies and Westlind, |
|
Tree establishment under alternative silvicultural systems | Mortality | Varied | Ostry, |
Disease incidence | Varied | Ostry, |
|
Disease severity | Decreased | Rosenvald et al., |
|
Recovery | Varied | Filip et al., |
|
Canopy cover | Mortality | No data | |
Disease incidence | Varied | Campbell and Antos, |
|
Disease severity | Increased | Condeso and Meentemeyer, |
|
Recovery | No data | ||
Tree density | Mortality | Increased | Burdon et al., |
Disease incidence | Increased | McCracken and Dawson, |
|
Disease severity | Increased | Desprez-Loustau and Wagner, |
|
Recovery | No impact | Bishaw et al., |
|
Thinning | Mortality | Varied | van der Kamp, |
Disease incidence | Varied | Hungerford et al., |
|
Disease severity | Varied | Morrison et al., |
|
Recovery | Increased | Amorini et al., |
|
Diseased tree removal | Mortality | No data | |
Disease incidence | Decreased | Kanaskie et al., |
|
Disease severity | Decreased | Amorini et al., |
|
Recovery | No data | ||
Mortality | Decreased | Lavallee, |
|
Pruning and coppicing | Disease incidence | Varied | Hungerford et al., |
Disease severity | Varied | Ostry, |
|
Recovery | No data | ||
Mortality | Decreased (dependant on species mixture) | Heybroek, |
|
Species diversity and mixtures | Disease incidence | Decreased (dependant on species mixture) | Benedict, |
Disease severity | Decreased (dependant on species mixture) | Hantsch et al., |
|
Recovery | Increased (dependant on species mixture) | Gerlach et al., |
As explained above, the concept of primary infection [cf. Equation (1)] captures the pathways by which the pathogen enters the forest unit of interest. These primary infections can occur from other forest units, for example by wind or water movement of inoculum, from alternative hosts, by movement on machinery and other human-mediated activities, or by transmission from soil inoculum.
The importance of connectivity for the conservation of forest ecosystems at a landscape scale is well-recognized (Lindenmayer et al.,
The impacts of connectivity on tree diseases have predominantly been studied in coastal forests of California and Oregon (USA). Total forest area within a landscape, correlated with connectivity, predicted increases in incidence (Meentemeyer et al.,
Forest connectivity via spatial proximity (Condeso and Meentemeyer,
Many tree pathogens, in particular root rots, can persist in soils following tree felling. Siting new plantations on previously forested sites may therefore increase the risk of infection due to high inoculum load in the soil. Here the soil acts as an “external” reservoir of inoculum for primary infection to initiate an epidemic in a newly planted tree population. However, research into the effects of previous land use is limited, due to the relative rarity of studies into forests established on previously non-forest land.
Naturally occurring
While previous land use could be expected to affect forest resilience to tree diseases, research on this is rare, and the findings amongst published studies are not consistent. This is likely to be due to the large variation in previous land use types, and particulars of previous land management, amongst the studies. However, such research is likely to increase in relevance for rotational forest systems, where the previous species planted in the unit may be considered. In some countries, including the UK, new forests are also being planted on land not forested in recent history in order to increase carbon capture in response to climate change, and natural tree regeneration is occurring due to abandonment of agricultural land (Poyatos et al.,
Site preparation methods can either introduce pathogens into an area where they were not previously found or reduce forest resistance to primary infection and hence increase the initiation of local disease spread. Previously felled sites contain remnant stumps, root fragments and brash, which may be a source of primary infection through spread of pathogens over time (from a previous tree population to a new one). Nonetheless, stumps resulting from thinning or partial cutting can also act as a source of secondary infection within the current tree population. Although this coarse woody debris is important for forest biodiversity more generally (Hartley,
Root rots have the highest potential for management through stump treatment and have unsurprisingly been the subject of the greatest number of studies. Methods of stump treatment may be physical or chemical. Infection of forest stands by
There has been a long history of incidence of
In addition to retained stumps, root fragments from felled trees can act as reservoirs of pathogen inoculum. Few studies have reported beneficial effects of root removal, although Shaw et al. (
Prescribed or natural fire reduces pre-planting inoculum load through either burning of stumps, root fragments and woody debris, or through killing of the pathogen due to high temperatures. However, results from burning are not consistent. Naturally occurring fires in Californian coastal redwood and mixed-evergreen forests led to reduced isolation rates of
Fertilizer application has mixed impacts on disease severity. Increased damage by twisting rust fungus (
Overall, removal or treatment of tree stumps as a source or receptor of pathogen inoculum has a positive effect on forest resilience to tree disease, through reduced infection of trees retained on the site or newly planted trees. However, studies are concentrated on root rots. Stumps, and other dead wood material, are also known to be important in survival of populations of a number of invertebrate forest pests, and there is an evidence gap about their significance as a source of inoculum of a wider range of pathogens with airborne spores that infect the shoots of trees. We found that studies of root fragment removal and burning give more mixed results and are under-researched. A future research priority is to assess the trade-offs between reducing inoculum levels using such treatments and the damage they cause to retained trees (e.g., through wounding), which can increase their susceptibility to infection.
Secondary infection [cf. Equation (1)] refers to transmission of a pathogen between trees within a region of interest (forest unit). Secondary infection therefore captures the direct transmission component of epidemics that depends upon the number of currently infected individuals. Although this typically relates to an outbreak situation between trees of a similar age, of particular concern for forest management is secondary infection from mature trees to seedlings, often planted to form the crop in the next forest rotation. Actions that increase environmental stress on a tree, thus reducing its vigor, are also likely to increase the rate of secondary infection.
Effects of tree species mixture, i.e., planting two or more species rather than a monoculture, or increasing tree species diversity, i.e., through the number of species planted together or as an indirect result of other silvicultural actions, on forest resilience to tree diseases have been extensively studied, with good coverage of both tree and pathogen species in sites across Europe and North America. Tree species diversity effects have been the subject of recent review papers. These recognize that greater diversity is associated with decreased tree mortality caused by pests and pathogens, identifying reduced access to hosts and increased distance between hosts as potential mechanisms for reducing secondary transmission as an epidemic progresses (Pautasso et al.,
Summary of studies in tree species diversity/mixture effects.
General disease | General forest | Europe (multiple locations) | Forest tree diversity | No | Reduced disease incidence | Nguyen et al., |
Fungal infections | Broadleaf | Germany | Species richness | No | Reduced disease incidence in most susceptible species | Hantsch et al., |
Sugar maple | Canada | Tree diversity | No | Reduced disease incidence | Bergdahl et al., |
|
Oak forest | California | Species richness | No | Reduced disease incidence | Haas et al., |
|
Douglas fir | California | Tree diversity | No | Reduced mortality | Ramage et al., |
|
Silver fir | Spain and Italy | Pure vs mixed stands | No | Increased isolation of pathogen from soil in mixed stands | Oliva et al., |
|
Root rot | Lodgepole pine | British Columbia, Canada | Mixtures containing cedar and birch | Yes | Reduced mortality | Morrison et al., |
Root rot | Lodgepole pine | British Columbia, Canada | Mixtures containing Douglas fir | Yes | Increased mortality | Morrison et al., |
Eucalyptus | Australia | Mixture containing |
Yes | Reduced mortality (not seen with other |
D'Souza et al., |
|
Norway spruce | Norway | Mixture containing Scots pine | Yes | Reduced disease incidence | Linden and Vollbrecht, |
|
Fungal infection | Germany | Mixture containing Scots pine | Yes | Reduced disease incidence | Hantsch et al., |
|
Fungal infection | Germany | Mixture containing Norway spruce | Yes | Increased pathogen load | Hantsch et al., |
|
Fungal infection | Germany | Mixture containing European beech | Yes | Increased pathogen load | Hantsch et al., |
|
Ash dieback | Ash | Czech Republic | Mixture containing |
Yes | Reduced disease severity at stand level | Havdova et al., |
Ash dieback | Ash | Czech Republic | Mixture containing oak species | Yes | Increased disease severity at stand level | Havdova et al., |
Douglas fir | USA | Mixture containing conifers | Yes | Increased mortality | Gerlach et al., |
|
Douglas fir | British Columbia, Canada | Mixture containing conifers | Yes | Increased mortality | Baleshta et al., |
|
Scots pine | Finland | Mixture containing aspen and willow | Yes | Increased disease incidence | Mattila et al., |
|
Scots pine | Finland | Mixture containing aspen | Yes | Increased mortality | Mattila, |
|
Fungal infection | Mixed forest | Germany | Mixture containing |
Yes | Increased pathogen load | Hantsch et al., |
Willow | Ireland | Clone diversity | Yes | Reduced mortality for most susceptible clones | McCracken and Dawson, |
|
Willow | Ireland | Clone diversity | Yes | Later disease onset within stands under 4 years old | McCracken and Dawson, |
|
Willow | Northern Ireland | Clone diversity | Yes | Increased growth rate | McCracken et al., |
|
Willow | Northern Ireland | Clone diversity | Yes | No change in mortality, but higher growth in the first 3 year harvest cycle | Begley et al., |
There is general agreement across studies that increases in tree species diversity are associated with an increase in forest resilience with respect to invasive pathogens. In sites across Europe, more diverse forests were associated with lower levels of disease incidence (Nguyen et al.,
Diversity amongst clones in monocultures can also affect resilience to tree disease. Willow rust (
An important mechanism cited for the benefit of species mixture is the dilution of trees of species susceptible to a given pathogen by individuals of non-host species. However, experimental results of this effect are variable, and the specific composition of species in a mixture is found to be important. In an experimental study in Minnesota with seedlings of six conifer and four hardwood tree species planted in three mixtures differing in the proportion of individual tree species, the relative proportion of susceptible conifers or resistant broadleaves had a significant effect on mortality associated with
There is variation amongst conifer species in their susceptibility to
Variation in the impacts of tree diversity on resistance to tree pathogens is likely related to tree species identity in the same forest unit (on a scale from individual adjacent trees up to ca. 50 m), with tree characteristics beyond simply host or non-host being important. Indeed, this may also be the main driver of any detected effects of species diversity within forest stands. Severity of infection of
In general, higher tree diversity improves forest resilience to tree diseases. However, a major mechanism in this effect has been found to be linked to the identity of the tree species present (i.e., species composition). Highly susceptible species show the largest reductions in pathogen presence and impact with increases in tree diversity. There is also evidence that greater benefit for such susceptible tree species can be obtained if they are mixed with trees not susceptible to the pathogen. It is important that future experiments are designed in a way that allows separation of effects due to species identity from those due to species diversity
For many tree species, planting or natural regeneration under shelterwood leads to better establishment than in open conditions (e.g., after clearcutting; Raymond and Bédard,
Across studies, the relative incidence of pathogen infection between shelterwood and clearcut sites shows high variation even within sites, and between tree and pathogen species. In study locations across the USA,
Amongst selection or retention systems, the size of felling gap has been suggested to influence forest resilience to tree diseases, but it is acknowledged that this varies with tree and pathogen species. The most rigorous experimental study was carried out in a pine forest in Minnesota (USA), in which
Understanding of the impacts of the range of alternative silvicultural systems on forest resilience to tree diseases is poor, with relatively few studies. It is not surprising that the available evidence shows little consistency across pathogen and tree species, given the wide variation in their transmission pathways and modes of infection. Transmission to seedlings of pathogens that spread via root contact is expected to be greater in shelterwood or other even-retention or small-gap selection systems. This effect may be less so for pathogens that disperse via airborne or water dispersal. Similarly, amongst trees, light-demanding species that show greatest vigor in open clearcut or large gap sites are likely to be less susceptible to infection in such site conditions. In contrast, more shade-tolerant species may be less susceptible in shelterwood or small gap systems where they are less vulnerable to environmental stress. However, such deductions, and in particular the net effects of any trade-offs between the effect of site conditions on the rate of pathogen infection and on the level of seedling vigor, need further empirical research. It can be expected that the net outcome will vary amongst tree and pathogen species.
Individual silvicultural systems differ from each other in several different component silvicultural operations and resulting stand conditions, which are addressed in turn in the sections below.
Differences in forest canopy cover at different stages of the forest growth cycle is one of the obvious distinctions amongst different silvicultural systems. It is also influenced by decisions over specific silvicultural operations, e.g., tree species selection, planting density, and thinning. Canopy cover affects microclimate, solar irradiation and air flow, all of which can alter the survival and dispersal of pathogens within a forest. Although it could not be distinguished as a separate effect in the reviewed literature, canopy cover would also be expected to affect movement of animal vectors of disease. We found only three studies explicitly investigating the impacts of canopy cover and their results conformed to the expectation for the different types of pathogen species, given that greater canopy cover is associated with higher air humidity, but lower sub-canopy wind speeds. Two studies in California mixed evergreen forest found a positive relationship between canopy cover and severity of infection by
High tree density reduces the distance between potential host individuals and would therefore be expected to increase rates of pathogen spread by secondary infection within a forest. This effect is likely to vary among pathogen species, with a greater effect seen for pathogens that spread via root contact than for those with only airborne dispersal. Dispersal via animal vectors is also likely to be affected by tree density, though this could not be distinguished as a separate effect in the reviewed literature. Variation in total tree density can result from many causes, e.g., initial density of planting or natural regeneration or reduction in density due to intensity of thinning or other forms of selective felling. Reduction in density of individual host species can occur as a result of mixture with other species (reviewed in section Tree Species Mixture and Diversity). Studies that reported on the effects of thinning as an operation are reviewed in the following section Thinning.
We found only one study testing the relationship between tree density and the incidence of a pathogen species that spreads through root contact. In Minnesota, USA, broadleaf and conifer seedlings were planted in several species mixtures in recently logged sites at four different densities, ranging from 0.25 to 2 m spacing. In this study the effect of closer spacing on mortality was not significant (Gerlach et al.,
High tree densities increase susceptibility to a broad range of tree pathogens, both those spread by root contact and airborne spores, although this effect is not universal, with many studies showing no relationship. It is likely that the relationship between tree density and pathogen prevalence is not linear but characterized by thresholds at both low and high densities. For most pathogen species forests with a high load are unlikely to see changes in pathogen spread through reduction in tree density, as the probability of secondary infection is likely to remain high even with relatively large distances between trees. Similarly, once distance between trees exceeds the normal dispersal distance of a pathogen, further increases in distance would be expected to have a smaller effect. We found no clear evidence of effects of forest structure
Thinning may be carried out as a planned action to increase production of the highest value timber from a forest, to improve other components of stand condition, or in response to damaging disturbance events, including tree pathogen outbreaks. In the latter case, thinning can take the form of salvage cutting, where dead or dying trees are removed, or sanitation cutting, which targets trees highly susceptible to disease, with the intention of reducing forest inoculum load. The latter type of thinning to remove susceptible trees will be considered in the next section Diseased Tree Removal. Thinning to improve growth or other components of tree vigor, through reduction in tree density (section Tree Density), could also be expected to improve resilience to tree diseases. However, studies show a large variation in forest response to thinning actions. Negative impacts could be attributed to the resulting stumps, whose cut surfaces are susceptible to infection (compare section Site Preparation), wounding of remaining trees, or due to increased traffic within managed areas, increasing pathogen spread by vectors (Jules et al.,
Studies of other species of root rot also predominantly show an increase in infection with thinning. In 15 year old
Thinning has highly variable effects on tree diseases besides root rots. The most frequently studied pathogens infecting tree shoots have been dothistroma needle blight of
As well as being a legacy of the harvesting of mature trees, stumps are also present throughout growing stands as a result of thinning operations. Chemical or biological treatment of stumps resulting from thinning can be effective at reducing pathogen incidence, as is the case for final harvest tree stumps (section Site Preparation). In Sweden, following thinning, the proportion of
In the majority of cases, forests that have undergone thinning have a higher incidence of tree disease than unthinned sites. However, results are variable, even within the same site, pathogen or tree species. Such variation likely arises not from thinning itself, but from other changes within the forest associated with thinning regimes. Pathogen loads can increase due to increased movement of machinery and human vectors into a forest to carry out thinning (Jules et al.,
Removal of diseased trees is often one of the criteria applied for tree selection in thinning of diseased stands. In some cases it is the sole focus of a control programme, either restricted to trees already showing disease symptoms or extended to trees considered to be at high risk of infection, e.g., because of their species and proximity to diseased trees. The effectiveness of this measure has been assessed in a number of studies, though not through rigorous experimentation. Examples include the spatial spread of Dutch elm disease (
Pruning of lateral branches is usually carried out to improve timber quality by reducing knots in the subsequent radial wood growth. Analogous to thinning, pruning may also be carried out to reduce pathogen incidence by targeting infected or susceptible damaged branches or to reduce sub-canopy humidity in the forest. However, pruning wounds also create potential sites for pathogen entry and, as with thinning, pruning operations may increase traffic and potential of cross-infection on tools, acting as vectors of pathogens.
Positive impacts of pruning
For other pathogens, results of pruning have not been so positive. Pruning increased
Shoot removal to reduce multiple stems to a single stem was carried out on
Pruning, coppicing and shoot removal have a highly variable impact on resilience of forests to tree pathogens. Some of the literature on the subject points to an increase in susceptibility caused by pruning wounds and increased vector or air movement of the pathogen within the forest. However, other studies show a decrease in susceptibility to some pathogens, linked to removal of susceptible branch material and reduced sub-canopy humidity. There is a lack of experimental studies that enable testing of these mechanisms and their trade-offs. While pruning is less common as a forest management practice than is thinning, it should be a priority for future studies. There is good potential to link knowledge of the effects of pruning practice on tree pathogens in arboriculture with the evidence required to inform forest management. A priority is to understand more about what controls the risk of entry into pruning wounds of the main airborne pathogens of commercial tree species.
The processes described above in terms of primary and secondary infection capture the first element of forest resilience, its resistance to an invading pathogen. The second element, the capacity of the forest to recover, is discussed in this section. As explained above, we considered rates of tree growth and natural regeneration following the onset of pathogen infection, which were the only measures of the recovery of the forest ecosystem reported in the reviewed studies. Within our working definition of resilience, we did not include changes in pathogen inoculum or infection level in the ecosystem as measures of recovery, in order to avoid mixing up “cause” and “effect.” The capacity for forest ecosystem recovery can be assessed over a wide range of temporal and spatial scales. For entire managed forests it is extremely likely that, over the long term, the decisions of forest managers will be crucial in determining the rate and trajectory of forest recovery. Gibbs et al. (
In a large experiment in British Columbia forests subject to infection by
In a complex mixture experiment of many
Inoculum removal prior to planting has had mixed effects on subsequent tree growth. A large-scale experiment in a British Columbia forest infested with the root pathogens
There are insufficient studies of alternative silvicultural systems to draw any clear conclusions about the implications for recovery. In
In a
Studies of thinning impacts have consistently shown that it results in increased tree growth rates in infected stands sufficient to promote forest recovery. In
One study was notable for providing evidence of natural regeneration as a process of forest recovery, but its results were mixed. In British Columbia selective cutting, a silvicultural treatment somewhat akin to thinning, in forests infested with
Published studies on forest resilience to tree diseases have uneven coverage with regard to geographical locations, management options, and pathogen species. The majority of studies have been restricted to a single forest area, while larger-scale studies often find inconsistent results across locations. This patchy coverage, and a lack of detail in reporting of the management options tested or the scale of their effects, hampers our ability to produce a systematic assessment of the similarities and differences in the impacts of management on tree resilience to different tree pathogens. Insufficient evidence is provided to enable comparison of effectiveness between options. Individual studies are limited to considering a single, or small number of related, pathogens, and therefore do not provide an adequate evidence base for forest managers who need to decide how best to increase forest resilience against multiple known and unknown future threats. Determining general conclusions to best inform forest management in the face of such a diversity of (and likely increasing pressure from) future pathogen risks is therefore challenging. Most management actions have been responsive, seeking to combat specific pathogens that are either established in a forest or new outbreaks after they have reached a region. Interventions thus tend to focus on reducing sources of inoculum or the rate of secondary infection, including the transmission of inoculum and the susceptibility of trees. Because most studies have researched forests managed for timber production, their evidence should not simply be extrapolated to forests managed for other benefits (for which different measures of resilience, linked to other ecosystem services, would be more relevant).
Although the published studies included in this review were very uneven in their coverage and did not produce consistent results, they provided stronger evidence of the benefit of certain management options for forest resilience to pathogens. The reduction of primary infection by limiting the connectivity of forest units and by the removal or treatment of stumps during site preparation, and the reduction of secondary infection by planting mixed species forests, are the management options with the strongest evidence for improving forest resilience to pathogens. Despite this, in each case the effects are strongly modified by the particular methods used and tree species involved, so this evidence can only be taken as a first indication to inform management decision-making. Forest managers must also consider the scale of the effect of each management option and trade-offs with other impacts on the forest system, such as the effects on environmental conditions and thus tree health and vigor.
Commercial timber production is the dominant management objective in the studied forests, with the need to reduce the risk to this posed by tree pathogens and pests increasingly recognized. However, even in commercial forests biodiversity conservation is also an increasingly important objective. Therefore, the potential negative impacts of connectivity on risk of spread of pathogens and pests needs to be weighed against the demonstrated benefits of higher connectivity for biodiversity (Lindenmayer et al.,
Perhaps the most consistent finding of the reviewed research, supported by multiple studies across a range of pathogen species, although still not ubiquitous, is that the rate of secondary infection of trees of a given species is reduced if these trees are growing in a mixed, species-diverse forest rather than a monoculture. In this sense, higher species diversity has an insurance value against future income risks due to disease, which will be positively valued by risk-averse forest managers (Finger and Buchmann,
In seeking to achieve the most economically efficient solution to exploiting the benefits of higher tree species diversity for increasing forest system resilience to tree pathogens, a key consideration is the spatial scale at which such mixing occurs. If the economic benefit of including within the forest a portfolio of different tree crop species can be achieved by establishing large monoculture blocks of each species, then this may only cause a small increase in management costs compared with a whole-forest monoculture. However, knowledge of ecological mechanisms would suggest that the larger the monoculture blocks the smaller will be the ecological benefit through diluting the individual trees of susceptible species. It is also possible that resilience of susceptible trees is increased due to interaction with other tree species, which is unlikely to occur if mixing takes place only at the landscape scale (Bauhus et al.,
With reference to recovery of forest ecosystems, there are a number of studies of the effects of silvicultural treatments on the growth of mostly conifer crop trees in pathogen-infested forests. The results generally indicate that tree growth increased following silvicultural treatments, irrespective of the fact that the studies were carried out in forests where the trees were subject to pathogen infection. However, there are very few studies reporting on the effect of silvicultural treatments on forest recovery through natural regeneration.
The findings of this review have several implications for epidemiological modeling of emergence, spread, and persistence of tree pathogens and for capturing the resilience of forests in response to such threats. However, we identified many important evidence gaps in the empirical literature that should be a priority for new primary research to fill. Our review aimed at providing a foundation for linking the processes and parameters used in models, specifically the epidemiological components of primary and secondary infection, and the ecological components of forest recovery, to the published observational and experimental data. This has several important implications for this area of modeling. Firstly, while our review showed the importance of tree species mixture effects, most models consider a forest comprising only a single host species (Kleczkowski et al.,
We hope that this paper will contribute to a dialogue between forest managers and ecologists on one hand and epidemiological and bioeconomic modelers on the other, to establish criteria for experimentation that can be used to better parameterize models and rigorously test their results.
All datasets generated for this study are included in the article/
JH conceived the study. AK, NH, CG, and JH acquired funding for the project. JH and MR designed the study. MR carried out data collection, performed the analysis and led the drafting of the manuscript, with input from JH. All authors discussed and interpreted the results and contributed to the writing of the final manuscript.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The authors thank the other members of the FOREMOD project team (Chris Quine, Morag Macpherson, Ciara Dangerfield, and Oleg Sheremet) for valuable discussions and insights which have contributed to the development of this paper in many ways.
The Supplementary Material for this article can be found online at: