Get 20M+ Full-Text Papers For Less Than $1.50/day. Start a 14-Day Trial for You or Your Team.

Learn More →

Anthropogenic Disturbances and the Emergence of Native Diseases: a Threat to Forest Health

Anthropogenic Disturbances and the Emergence of Native Diseases: a Threat to Forest Health Purpose of Review Human-caused global change is fundamentally altering natural forest ecosystems. More trees are exhibit- ing a wide range of symptoms indicative of poor vigour, particularly stressed species at the edge of their native ranges and stands growing on marginal sites. This review will focus on complex tree diseases (declines) caused by native pathogens and the key environmental drivers that contribute to this phenomenon. These systems are frequently complex, with multiple drivers at work. Recent Findings Using four cases studies on different continents, we explored the direct and indirect environmental drivers underlying these decline syndromes. Although climate and weather events seem to be usually associated with forest decline, we found that environmental disturbance by either forest management or land-use changes is also a global predisposing factor of decline which deserves more attention. Changes in land use have directly benefited pathogens such as root rots in the Pyrenees (Spain) or indirectly by making the environment more conducive for canker and foliar diseases in Australia and the USA. Focus on land-use changes could improve understanding of current decline problems such as those affecting Araucaria in Chile. Summary The next century will almost certainly see an unprecedented rise in forest pathogen epidemics, requiring a proac- tive rather than reactive response. Diseases caused by native pathogens with complex aetiologies will become more common, and recognising, characterising and managing these epidemics are difficult because native pathogens are frequently already widespread, and eradication is not feasible. We need to start approaching these issues from a ‘whole ecosystem’ perspective, highlighting the many aspects and entanglements of forest declines and allowing us to respond with management options tailored to each scenario. The approach proposed here provides logical steps based on six questions to untangle the direct and indirect environmental drivers of tree declines. Keywords Abies alba · Araucaria araucana · Corymbia calophylla · Global change · Pinus strobus · Tree decline This article is part of the Topical Collection on Forest Pathology * Treena I. Burgess School of Biological Sciences, University of Canterbury, t.burgess@murdoch.edu.au Christchurch 8041, New Zealand Department of Plant, Soil and Microbial Sciences Harry Butler Institute, Murdoch University, Murdoch 6150, and the Department of Forestry, Michigan State University, Australia East Lansing, MI 48824, USA Forestry and Agricultural Biotechnology Institute Forestry and Agricultural Biotechnology Institute, Department of Plant and Soil Sciences, University Department of Biochemistry, Genetics and Microbiology, of Pretoria, 0002 Pretoria, South Africa University of Pretoria, 0002 Pretoria, South Africa Deparment of Crop and Forest Sciences, University of Lleida, 25198 Lleida, Spain Joint Research Unit CTFC-AGROTECNIO-CERCA Center, 25198 Lleida, Spain Vol.:(0123456789) 1 3 112 Current Forestry Reports (2022) 8:111–123 barriers are crossed. There are numerous examples of this: Introduction sudden oak death in the western USA [9], chestnut blight [10], Phytophthora dieback in the southwest of Australia Forest systems are experiencing unprecedented transforma- [11], Dutch elm disease [12] and Ash dieback [13]. tion rates due to many disruptions related to global change, Pertinent to this review, native pathogens do not need to including land clearing and fragmentation, severe droughts overcome geographical or evolutionary boundaries. How- and wildfires and outbreaks of invasive alien pests and ever, the environmental barrier may be overcome due to pathogens [1]. Several reviews have explored these topics. land-use change and/or overarching climate change, lead- However, one gap in the current literature is exploring how ing to situations where native pathogens exhibit increased anthropogenic disturbances lead to the emergence of native pathogenicity to co-evolved hosts. For example, selective pathogens resulting in disease epidemics more typical of logging or clear-felling coups can result in an even-aged invasive alien pathogens. Understanding and teasing out monoculture of a native tree species that is now equally sus- the drivers of native epidemics in forest ecosystems will •• ceptible to specific pathogens [14 , 15]. The environment aid in mitigating this problem. As eradicating ubiquitous can alter host–pathogen relationships, and depending on the native pathogens is not an option, management strategies region, climatic conditions may become more or less favour- must focus on ameliorating ecosystem stress, a complex able for pathogens. Weather (short-term atmospheric con- undertaking. ditions) and climate (weather of a specific region averaged Disease is a consequence of a virulent pathogen, a suscep- over a long time period) both impact pathogens, their hosts tible host and a conducive environment (i.e. the disease tri- and their interactions. Climate change refers to long-term angle [2]). Trees in natural ecosystems are mixed in age and changes in climate. For example, climate change leading species composition, and the impact of pathogens adapted to to long-term drying is a chronic change while drought is a particular host or life stage is limited by the availability of an acute change; both may favour pathogens by enhancing resources [3]. Natural ecosystems are, typically, in balance their fitness or driving expansion in distribution ranges and/ with their native pathogens, and severe disease outbreaks or exerting stress on tree hosts, predisposing them to disease are rare [4]. However, this co-evolution occurred over time •• development [16 ]. and within an environmental envelope [5]. Human activities Perhaps, the first to highlight the role of climate in forest have disturbed this natural balance between trees and their disease was Hepting [17], who concluded that a severe out- co-evolved pathogens, reducing ecosystem resilience. These break of a native pathogen ‘is a rare removal by the weather of activities include land clearing and fragmentation, leading obstacles that ordinarily constrain the pathogen’. In an era of to more edges exposed to climatic fluctuations and other global change, the disease triangle must be updated to consider stressors such as increased run-off or pesticides from agri- the environmental component in two timeframes: the weather, culture. Harvesting of trees, selective or clear-felling, alters which must be conducive to disease development, and overall age class and species composition, and hence the availability climate change and the underlying stress it causes [18]. The of susceptible hosts. This complex interplay between natural disease triangle only explains the point at which disease is ini- resilience and increased stressors can lead to native patho- tiated and the subsequent symptoms that develop (acute); other gens causing disease epidemics as impactful as those typi- models (such as Manion’s decline spiral) treat tree disease in cally seen for invasive pathogens. In addition to these direct a more holistic space taking into account other interactions of impacts by human activities, the impacts of anthropogenic the host and pathogens. The concept of chronic tree disease or climate change are increasingly experienced in forest sys- tree decline caused by interchangeable predisposing, inciting tems, with this further contributing to disease development and contributing factors was first proposed by Sinclair [19]. by native pathogens. Manion [20] developed this concept further and proposed the The study of emerging infectious diseases has its his- tree disease spiral and later the decline disease spiral [21]. The tory in medical and veterinary fields but has also applied to early 2000s saw a rise in studies and reviews of challenges to plant pathogens [6]. Three barriers limit the development of forest health in the face of globalisation and climate change [6, emerging infectious diseases: geographical, environmental 22, 23]. Drought, in particular, was seen as a significant driver and evolutionary (compatibility) (for detail, see Paap et al. of disease emergence. [7]). Release from any of these barriers can result in disease The impact of invasive alien forest pathogens is well development. In the context of invasive alien pathogens, documented; this review will concentrate on complex tree globalisation (trade leading to accidental movement of for- diseases (declines) caused by native pathogens in the era of est pathogens to naïve suitable hosts) allows pathogens to anthropogenic global change. As elucidated by three case overcome geographical barriers [8]. If this leads to oppor- studies, we explore the key environmental drivers behind tunities for microorganisms to encounter naïve hosts lacking this phenomenon, showing that these systems are often co-evolved resistance, then the evolutionary/compatibility complex, with multiple drivers involved. Finally, using 1 3 Current Forestry Reports (2022) 8:111–123 113 Fig. 1 Quambalaria coyrecup causing cankers on Corymbia calophylla. Left, leading to branch dieback and death of roadside trees; centre, extensive perennial cankers; right, sporulation of Q. coyrecup on the canker surface the decline of Araucaria araucana in South America as [26]. This habitat loss has resulted in forest fragments inter- an example, we recommend an experimental approach that spersed amongst various land-use types [27]. Forest fragments could be applied to understand the dynamics of emerging have distinct edge habitats that experience different envi- forest pathogen outbreaks. We highlight the need for this ronmental conditions compared to the interior of fragments approach to consider both temporal and multi-spatial scales. [28–30]. Specifically, highly fragmented areas in SWWA have resulted in remnant tree stands dominated by C. calophylla, and these fragmented areas are surrounded by die ff rent types of land Marri Canker; Pathogen: Quambalaria use (e.g. road and land used for horticulture, agriculture, viti- coyrecup, Host: Corymbia calophylla culture or grazing). It is in these highly fragmented areas that canker incidence is highest. Forest edges only exposed to one Aetiology and Extent type of land use, and interiors of forest fragments have lower •• canker incidence than highly fragmented areas [31 ]. Quambalaria coyrecup is a basidiomycete smut-like fungus The SWWA has experienced dramatic climate changes. thought to be endemic to the southwest of Western Australia Rainfall has declined over the past 30 years, and in com- (SWWA), and it is the causative agent of stem cankers in Cor- bination with a growing population requiring increases in ymbia calophylla, a keystone Myrtaceae tree species endemic water demand, groundwater levels have declined [32]. The to SWWA [24]. Excessive bleeding (gummosis), staining region has also experienced heatwave-compounded drought limbs or trunks dark red, splitting and eventual shedding of events [33]. With both long-term precipitation reduction bark revealing perennial cankers and Q. coyrecup sporula- and drought, SWWA has experienced long-term drying, the tion as powdery white masses within the cankered area are impacts of which have already been observed in crown die- all symptoms of this disease [25]. As cankers progress, they back in dominant forest species, Eucalyptus marginata and eventually ‘girdle’ the affected limb or trunk, resulting in the C. calophylla [34]. This overall climate change is one of the death of the limb or death of the entire tree (Fig. 1). These abiotic factors driving canker incidence in C. calophylla. symptoms were first observed in C. calophylla in 1939–1940, but at the time were of no serious concern. In subsequent dec- Indirect Environmental Drivers ades, additional biotic and abiotic factors have caused changes in this native pathogen-host relationship. Such factors include Anthropogenic disturbance also changes soil microclimate, climate change, increases in habitat fragmentation and interac- which results in alterations in soil chemistry and compo- tions with invasive plant pathogens. By the 1990s, these stem • sition belowground [35 ] and plant diversity aboveground cankers were causing a noticeable decline of C. calophylla. •• [31 ]. Belowground processes and communities are highly sensitive to these changes, further predisposing C. calo- Environmental Drivers phylla to canker disease. For example, concentrations of key soil nutrients (i.e. nitrogen, phosphorus and potassium) are The SWWA is a highly fragmented landscape with increasing much higher along edge habitats where C. calophylla has a pressure from expansion in both agriculture and urbanisation • higher canker incidence [35 ]. In addition, communities of 1 3 114 Current Forestry Reports (2022) 8:111–123 Fig. 2 (Left) Decline of silver fir (Abies alba) in the Pyrenees. (Centre) Leading to defoliation and tree mortality. (Right) Mortality is associated with a widespread presence of root rots such as Heterobasidion abietinum amongst other pathogens beneficial mycorrhizal fungi have lower richness and diver - timing and length of droughts within these environments are sity in edge habitats in comparison to forest habitats [35 ]. also important in disease development [42]. Fragmented forests can experience greater pressure from invasive plant pathogens [36]. Phytophthora spp. Summary have caused devastation to forests in SWWA, especially the invasive Phytophthora cinnamomi [37]. Landscape- Overall, the decline of C. calophylla seems to have been scale surveys identified that C. calophylla present on sites instigated by anthropogenic disturbance but is a complicated infested with pathogenic Phytophthora species had higher decline involving changes both above- and belowground. levels of canker incidence [38]. Glasshouse studies also Specifically, a drying climate combined with habitat frag- showed C. calophylla co-infected with Phytophthora spp. mentation and the indirect effects of habitat fragmenta- and Q. coyrecup were more stressed than C. calophylla tion (i.e. changes in soil nutrients and biotic communities) infected with Q. coyrecup only [39]. To add to the com- predisposes C. calophylla to canker disease caused by Q. plexity, the loss of ectomycorrhizal fungal diversity could coyrecup. play a role in Phytophthora spp. infection [40]. Together, these changes in abiotic and biotic characteristics of the soil are highly correlated with increased disease incidence Silver Fir Decline; Pathogens: Various, Host: in C. calophylla [35 ]. Abies alba Aboveground, anthropogenic disturbance has altered for- est stand structure where highly fragmented areas have dif- Aetiology and Extent ferent overstory composition than the interior of forest frag- •• ments [31 ]. Interior forest fragments consist of mixed E. The health of silver fir (Abies alba) in the Pyrenees (moun- marginata and C. calophylla overstory; E. marginata may be tain range straddling the border of France and Spain) has less tolerant to fragmentation as this species is not present in been of concern for the last three decades (Fig. 2). Several highly fragmented areas (however, E. marginata is removed stands in the southern side of the Pyrenees started showing by selective logging practices). In either case, the loss of signs of decline associated with the severe droughts occur- diversity in highly fragmented areas may have led to levels ring in the 1980s [43]. A large-scale pathological system- of pathogen pressure of Q. coyrecup above those which C. atic sampling revealed a high incidence of root rots such as calophylla is adapted to in their natural forest setting [41]. Heterobasidion annosum (42% of the stands) and Armil- The impacts of anthropogenic disturbance on C. calophylla laria spp. (93%), canker pathogens such as Melampsorella health can also interact with climate and drought events. Cli- caryophyllacearum (55% of the stands) or parasitic plants •• mate plays a major role in the development of cankers in C. such as Viscum album [44, 45 ]. At a Pyrenean scale, the calophylla. For example, cankers have been observed across parasitic plant Viscum album was the biotic agent most •• most of the range of C. calophylla, but areas with wetter and clearly associated with symptoms of decline [45 ]. Con- cooler climates have high incidences of canker [38]. The cerning the root rots, there is no information on the severity 1 3 Current Forestry Reports (2022) 8:111–123 115 of those pathogens and how much they increased in associa- been subjected to major shifts in temperature and precipita- tion with the decline process; however, the observed inci- tion, leading to increased drought and the decline of different dences (> 40%) are far greater than those observed in natural species. Silver fir in the Pyrenees has experienced a series of forests [46]. Later work on specific pathogens showed that droughts [53], much more severe than in other populations both H. annosum s.s. and H. abietinum affected fir stands, in the Alps or Romania [54]. although the latter was far more abundant [47]. Several spe- cies of Armillaria were also found affecting fir forests, with Indirect Environmental Drivers A. ceptistipes being the most abundant and the one associ- ated with higher defoliation. Aggressive Armillaria species Drought alone could not explain the phenomenon of decline such as A. ostoyae or A. gallica were more associated with and it was clear that it involved the effect of previous manage- fir-accompanying species such as Pinus uncinata or Fagus ment. Declining stands showed many more growth releases sylvatica than with fir decline [48]. than non-declining stands [43]. Management did not affect Later studies in more localised declining stands revealed all species similarly, and some species growing near silver fir high local severities of pathogens such as Amylostereum stands, such as Pinus sylvestris, benefited from it [55]. chailletii and Trichaptum abietinum, together with the Another critical aspect is the selection of trees to remain •• above-mentioned root rots [49 ]. Some interactions after logging. Trees showing symptoms of decline in the between the identified pathogens were found. For instance, 1980s were those growing slower at the beginning of the V. album was more prevalent in forests attacked by H. abi- century and before harvesting in the second half of the •• etinum [47]. Other secondary pests such as bark beetles from century [49 ]. Harvesting extracted the best and most vig- the genus Pityokteines have been associated with mortality orous trees and left those suppressed or co-dominant, prob- •• in declining forests [45 ]. ably with less capacity to adapt to the increased density and competition with the new cohort for the scarce water •• Environmental Drivers supplies [45 ]. Management triggered structural changes that contributed to forest decline appearing decades after. Fir forests were subjected to major logging during the sec- ond half of the twentieth century. During the selective log- ging process, some trees were left, and this caused massive Summary regeneration underneath. Thereafter, most of the fir stands remained untouched, and encroachment and competition Evidence shows that logging was the predisposing fac- were paramount. Thus, the most common forest structure tor for the decline of silver fir in the Pyrenees. Logging •• comprises two cohorts [45 ], with trees belonging to the during the second half of the twentieth century favoured older cohort showing the most symptoms of decline. In most root rot pathogens and dramatically changed the structure cases, the current land use involves a lower anthropogenic of the forest, leaving the weaker trees remaining in the pressure than in the past, allowing the forest to expand to stands. After harvesting, forest management mainly was areas previously used as grassland or crop areas [50]. Across stopped, and encroachment and high tree-to-tree competi- the Pyrenees, the abundance of Armillaria and Heteroba- tion caused stress to the remaining trees. Amongst those, sidion in dead trees and stumps and the abundance of Armil- decline affected co-dominant and suppressed trees left from laria in soil were associated with higher intensity logging the previous rotation. The droughts in the late 1980s were [47, 48]. The current prevalence of Heterobasidion is pos- an inciting factor for the decline, and it was then when the sibly inherited from the previous land use as no stump pro- crown condition of fir started deteriorating. Since then, mor - tection methods such as urea, Phlebiopsis gigantea or borate tality has affected the largest trees, where secondary pests were applied at that time. Viscum album showed a similar and pathogens contribute to tree death. association with former management practices, more preva- lent on those isolated trees with large diameter and opened crowns [47]. There is no information on the association of Amylostereum with forest fragmentation in the context of Caliciopsis Canker; Pathogen: Caliciopsis fir decline. However, it is known that wasps carrying the pinea, Host: Pinus strobus pathogen affect stressed trees [51]; therefore, the presence of the pathogen is probably associated with trees left after Aetiology and Extent the logging, the ones suffering the most considerable growth losses over the last century [52]. Pinus strobus (eastern white pine) will naturally regenerate The Pyrenean population of silver fir is the southernmost and tolerate a range of soil types and is utilised commer- distribution of the species in Eurasia. The Pyrenees have cially for lumber. Caliciopsis pinea is a canker pathogen 1 3 116 Current Forestry Reports (2022) 8:111–123 Fig. 3 Caliciopsis canker symptoms on Pinus strobus (eastern white cankers more evident when the bark is removed (photo credit centre pine): left, reddish flagging branches; centre, resinosis indicative of and right, James Jacobs, USFS) numerous cankers; right, numerous, small and sometimes cracking of P. strobus native to North America, with fruiting bodies Caliciopsis canker, and the disease has been associated with of C. pinea first reported in New York in 1880 [56]. Subse- regeneration (seedlings and saplings), pole timber mortality •• quently, Caliciopsis canker disease was reported as a ‘minor’ and sawtimber degradation [58 , 62]. canker disease with a ubiquitous distribution throughout the Seasonal projections forecast warmer, wetter springs and range of P. strobus [57]. Reports of Caliciopsis canker on winters coupled with dryer, hotter summers [63, 64]. Col- P. strobus have increased in severity and distribution in the lectively, these climate changes lead to conditions favourable last 20 years, particularly in the northeastern USA (New to pathogen reproduction and dissemination in the spring, England) and southeastern USA (the Southern Appalachian improved overwintering survival of pathogens and increased •• •• •• Mountains) [58 , 59 ], where regeneration and plant- water stress in the host during the summer [65 ]. Increased ing strategies have led to dense stands of P. strobus. The temperature and precipitation has been linked to the emer- disease is characterised by excessive resin production and gence of needle cast pathogens [66], and increased tempera- reddish sunken cankers on stems and branches as well as tures have been linked to increased severity of Caliciopsis •• •• bark fissures, crown thinning and dieback (Fig.  3) [58 ]. canker disease [59 ]. Serious canker disease and declining P. strobus have now been observed in the Great Lakes region of Michigan and Indirect Environmental Drivers Wisconsin, and recent surveys (2018–2019) have high- lighted the extensive distribution of the disease in these Pinus strobus is widely distributed across eastern America states. Caliciopsis pinea is a threat to P. strobus throughout on many soil types. Disease severity and incidence have not its native range, and the risk it poses to other hosts remains been associated with ecoregions, plant hardiness zones, slope •• •• •• unquantified [58 ]. or aspect [58 , 59 ]. Compared to well-drained, more fer- tile soils, disease incidence increased on sites with exces- Environmental Drivers sively or poorly drained soils, and disease severity increased •• on sites with nutrient-poor, excessively drained soils [58 ]. Management decisions facilitating the growth of P. strobus Disease incidence and severity were also higher in drier and on poor quality sites combined with a subsequent lack of shallow soils when compared to loamy soils [67]. management resulting in dense even-aged stands have led Costanza et al. [68 ] uncovered regional synchrony in to favourable conditions for the emergence of the native the timing of canker incidence and severity across different C. pinea. More specifically, replanting and regenerating P. sites; tree declines triggered by climate stress events (i.e. strobus on logged and abandoned agricultural and pasto- drought and flooding) occurred 1–3 years before canker ral land, coupled with a lack of management and fire sup- development. Disease severity is also positively associ- •• pression, has led to overstocked, even-aged stands on com- ated with mean annual temperature [59 ]. Climate change pacted and plough pan soils that restrict root penetration likely has wide-ranging impacts across broad geographical [60, 61]. Together, these factors are driving the emergence regions, and local differences in incidence and severity of C. pinea. All age classes of P. strobus can be impacted by may be exacerbated by poor site and stand conditions. 1 3 Current Forestry Reports (2022) 8:111–123 117 Other biological pests and pathogens such as a native scale Araucaria Decline: an Emerging Disease insect and a complex of native foliar fungi are thought to com- of Natural Forests in South America pound climate, stand and site stresses. The herbivorous insect Matsucoccus macrocicatrices pierces P. strobus bark and feeds A newly documented decline of Araucaria araucana on the sap, creating numerous wounds that are thought to add (Araucaria, Pewén or the Monkey Puzzle tree) emerged stress to the tree and facilitate the entry of C. pinea [69]. How- between 2015 and 2016 (Fig.  4). This tree species is ever, M. macrocicatrices has only recently been associated with endemic to the south-central Andes Mountain range slopes C. pinea cankers [69, 70] and was previously considered benign. in Chile and Argentina and the coastal range of Chile. Therefore, the association between Caliciopsis canker disease Field surveys undertaken inside its natural range at dif- and M. macrocicatrices is unclear. White pine needle pathogens ferent locations identified symptomatic trees in all visited (Lophophacidium dooksii, Lecanosticta acicola and Bifusella areas. A broad initial description of symptoms consistently linearis) are native foliar fungi that cause premature needle loss identified dieback of portions of the crown of trees with [71], with disease severity linked to warmer and wetter seasons the death of a small proportion of young trees (between [61, 66], with associated host mortality exacerbated by site and 1.5 and 3 m), and, in rare cases, death of full adult trees stand characteristics and the presence of Caliciopsis canker dis- [73, 74]. Knowledge of this new disease is still scarce, and ease [68 ]. the factors driving its emergence are not understood. Sur- veys at different sites (latitudes) across the Andes distribu- Summary tion have shown the most prevalent symptoms to be can- kers on branches and stems. These cankers slowly girdle Overstocking, deficient soil conditions (poor drainage, nutrient- healthy-looking branches and stems, causing the death of poor, shallow), pests and pathogens are linked with increased the affected organs. A fungus residing in a novel genus and Caliciopsis canker disease incidence and severity. Younger, species, Pewenomyces kutranfy, was found to be the causal smaller trees are more impacted than larger trees, and inad- agent of these cankers [74]. This pathogen is believed to equate soil water and excessively shallow-rooted trees are more be native as it has not been found elsewhere and is clearly likely to be impacted during drought events. In general, selecting adapted to the cold temperature characteristic of high-alti- sites with deep, sandy, well-drained soils and stand thinning at tude environments. While evidence suggests this fungal prescribed size classes is recommended to increase tree vigour, canker disease is the prevalent disease associated with the resilience and resource availability [72]. Caliciopsis canker has dieback observed in A. araucana in the Andes [74], sites now been observed in the Great Lakes region in Michigan and exist where cankers are only scarcely observed and where Wisconsin. Disease severity is currently lower than observed in other abiotic factors and biotic agents seem predominant the eastern states, and current research focuses on documenting [75]. The observation of both cankers and other symptoms the distribution, impact and epidemiology in the Great Lakes suggests that different disease syndromes may be present region. in different sites (populations). Fig. 4 Decline of Araucaria araucana in Chile: left, crown symptoms on adult trees; centre, dieback of branches associated with girdling can- kers; right, cankers on branches caused by Pewenomyces kutranfy 1 3 118 Current Forestry Reports (2022) 8:111–123 This decline may be driven by changes in weather, includ- Recommendations for an Experimental ing several years of intense drought [76], a rise in maximum Approach to Studying Emerging Native and minimum temperatures and a reduction in snow precipita- Diseases tion and persistence (also increasing drought in the following summer) [77]. Araucaria forests have a long history of anthro- Here, we detail the steps of an experimental approach pogenic disturbances, including an intensive reduction in for- (Fig. 5), with an outline to the approach rather than describ- est area since the arrival of Euro-American settlers through ing all the possible factors to be explored, as we believe intentional fires for clearing lands for grazing [78 , 79] and the outcome of each progressive step will guide the next intensive logging [80]. Most of the Araucaria forests were step. We encourage the inclusion of multidisciplinary teams, protected in the 1900s to ameliorate this reduction; however, encompassing at least forest pathologists, landscape ecolo- the disturbance has continued in parts of their distribution. gists, plant physiologists, soil scientists, climate modellers Overgrazing and cattle ranching [81], the introduction of alien and biostatisticians as deemed necessary, as efforts to under - mammals [82] and the increasing establishment of planta- stand and mitigate these declines require a detailed under- tion forests have further contributed to the fragmentation and standing of multiple factors and potential mitigation options. alteration of fire regimes [83, 84]. These disturbances have been shown to impact the health and regeneration capacity of Step 1. Is a single pathogen consistently associated the species. However, no large-scale studies have examined with the symptoms, or is there a more complex decline the link between these factors and tree health status. Conse- without a specific pathogen as a key component? quently, the potential importance of these factors as drivers of this recently emerged decline remains unknown. Studying Systematic surveys of symptomatic and asymptomatic trees a new decline such as this across a large area and in rugged should be undertaken at multiple locations to develop an under- terrain is challenging. Below, we develop an experimental standing of the disease aetiology, including disease progression, six-step approach to untangle the dynamics of complex tree and if a primary pathogen/s can be consistently observed or declines. not. The inclusion of specialists on different pathogens would increase the likelihood of correctly diagnosing the disease-caus- ing agent. The possibility of involvement of multiple pathogens, Fig. 5 An experimental approach to understanding a forest decline syndrome based on six key questions 1 3 Current Forestry Reports (2022) 8:111–123 119 the simultaneous emergence of disease syndromes and/or a gen- plot, canopy cover, sunlight penetration, slope, aspect, pH, eral underlying decline deserves careful consideration at this soil moisture). These variables can be used in linear model- initial stage. ling approaches to see which are significant in predicting In cases where a primary pathogen is found, answer- the health parameters of the populations. Surveys can be ing questions regarding its origin and biology may become conducted to determine disease incidence in sites experi- relevant, such as whether it is native or alien, or whether encing these disturbances or not (i.e. comparative study it has arisen through an evolutionary process (hosts jump, design). Surveys can include comparing damage inside/ host shift or host range expansion). Suppose a diversity of outside protected areas, comparing areas with contrasting secondary pathogens are detected. In that case, a stronger management histories (e. g. wood extraction, grazing, oth- emphasis should turn towards the host’s condition, looking ers; policy changes) and comparing sites where restoration at whether there are any evident localised abiotic drivers or programmes may have been implemented (e. g. planting, stressors, or if a broader range complex condition may be removing alien vegetation and animals). Alternatively, a underlying, i.e. Manion decline spiral. historical reconstruction of the forests (30–50–80 or longer years ago) can be included, combining information such as Step 2. Is this a local or large-scale problem? land-use changes, forest adaptation to human perturbation events or regimes still present or interrupted, and/or changes Systematic surveys should be undertaken at a larger in forests management. scale (ideally across the entire host range) to understand the scale of the issue. For example, is it occurring in a Step 4. Have there been changes in short- and/or long- single stand, multiple stands or across the entire distribu- term climate and/or weather conditions? tion range of the host? Assessing the consistency of symp- toms and pathogens needs to be considered by applying Climatic conditions can be considered at different tem- standardised and coordinated methods for disease charac- poral and spatial scales. Weather changes refer to short- terisation, scoring and sampling. Hyperspectral imaging term atmospheric conditions, while climate is the weather and other remote sensing tools could be considered [85]. of a specific region averaged over a long time. Historical Fungal population genetics studies can be used to assess (long-term) climate data for sites showing different levels if genotypes associated with disease differ from those in of disease/damage can provide evidence for correlation with asymptomatic trees [86] or if new genotypes have been trends in changing conditions such as changes in tempera- introduced to a region [87], well-planed hierarchical sam- ture (at different seasons) and precipitation (e. g. amount, pling can also determine if there is structure within popula- time and frequency of occurrence, type, persistence). Both tions [88]. Numerous population genetics studies have been long- and short-term changes can result in a disease out- undertaken considering invasive pathogens [15], but there break. Short-term weather data can be obtained in diverse are few examples with native pathogens. manners (weather stations, on-site temperature/humidity The presence of the pathogen across the range of the host recording devices such as iButtons) and combined with data and its isolation from asymptomatic trees provide strong evi- (e.g. plant composition, growth rate, tree health, ground dence for it being native rather than alien; this is an impor- cover, litter depth) from long-term monitoring plots. Any tant distinction as if it is an introduced alien pathogen, changes in weather at either a local or landscape scale could appropriate management goals should be determined, e.g. then be related to changes found in the type and amount assessment of eradication feasibility, development of con- of damage present. Plant-based indicators are an alterna- tainment and disease mitigation strategies [7, 89]. For native tive way to explore the change in climatic conditions and/ pathogens, the expectation is that they will have a ubiquitous or effect of such changes. These include, for example, stud- distribution, and management must focus on the release of ies of tree rings (which can link tree declines to changes in the stressors driving the pathogen emergence. atmospheric conditions) or taking leaf samples and using C isotopic signature (δ13C) to obtain information regarding Step 3. Is the disease associated with land-use change water scarcity. or human disturbance? Step 5. Have there been changes in other abiotic fac- For this purpose, landscape-level studies of disease tors? extent and distribution are required. Variables at this level include those related to human disturbance, e.g. distance to There are numerous additional abiotic factors, many of roads and hiking trails, changes in forest management (e.g. which may be linked to the anthropogenic changes observed changes in logging regimes), and air and water pollution in step 3, which may contribute to the incidence and severity and other plot variables (e.g. average age of individuals per of a disease outbreak. These include changes to soil structure 1 3 120 Current Forestry Reports (2022) 8:111–123 due to compaction or other factors, changes in fire regimes, ecosystem’ approach incorporates both biotic and abiotic increased nutrients or imbalanced nutrients due to fertiliser aspects of a forest community and the multiple interactions use, pesticide and herbicide damage, changes in soil pH, amongst host, pathogen, mutualists, the environment and increased salinity or altered drainage or water tables due to humans. A ‘whole ecosystem’ approach highlights the many land-use management. These geophysical and hydrophysical aspects and entanglements of forest declines and enables us changes will predominantly affect the host physiology and to respond with management options appropriate to each may reduce the hosts’ disease resistance. scenario. The framework proposed here provides a logical six-step approach to discovering the direct and indirect envi- Step 6. Have there been changes in other biotic fac- ronmental drivers of a forest decline syndrome. tors? Funding Open Access funding enabled and organized by CAUL and As with step 5, numerous potential biotic interactions its Member Institutions JO was supported by the ‘Ramón y Cajal’ fel- may influence a disease outbreak, and again many of these lowship RYC-2015–17459 from the Ministry of Science and Educa- will be linked to anthropogenic disturbance: changes in veg- tion of Spain. USDA Forest Service Forest Health Protection partially etation (stand structure, abundance, composition, density, supported MLS. basal area age) due to edge effects, invasion by alien plant species, other pests and diseases, rhizosphere biota changes Declarations and mycorrhiza. These other biotic impacts could also be the Conflict of Interest The authors declare no competing interests. result of climate, weather, land use, human disturbance and management and belowground changes and would indicate Human and Animal Rights and Informed Consent This article does not a complex interactive scenario, for example, rhizosphere- contain any studies with human or animal subjects performed by any of the authors. plant-pathogen interactions. Changes in belowground microbial composition can result from changes in soil condition and plant communities, Open Access This article is licensed under a Creative Commons Attri- which, in turn, can be affected by human disturbances and bution 4.0 International License, which permits use, sharing, adapta- tion, distribution and reproduction in any medium or format, as long changes in management. The most complex and challenging as you give appropriate credit to the original author(s) and the source, aspect of understanding tree declines with complex aetiolo- provide a link to the Creative Commons licence, and indicate if changes gies is attempting to unravel these relationships. were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not Conclusion permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a Due to global change, more trees will exhibit a wide range of copy of this licence, visit http://cr eativ ecommons. or g/licen ses/ b y/4.0/ . symptoms indicative of poor vigour, particularly in stressed species towards the limit of their native ranges and stands growing on marginal sites. By looking at four paradigmatic examples of forest decline, we found forest management had References a significant role as predisposing and inciting factors for tree health. Land-use change is one of the three components Papers of particular interest, published recently, have been highlighted as: of global change, including both climate change and glo- balisation, and more attention should be placed on its role • Of importance •• Of major importance on tree health. The prevalence of diseases caused by native pathogens with complicated aetiologies will increase, and 1. Ramsfield TD, Bentz BJ, Faccoli M, Jactel H, Brockerhoff EG. interdisciplinary teams are needed to untangle the multiple Forest health in a changing world: effects of globalization and biotic and abiotic causative factors and their interactions climate change on forest insect and pathogen impacts. Forestry. to reveal the primary drivers of the decline. Recognition, 2016;89:245–52. 2. Agrios GN. Plant Pathology. Fifth ed. Elsevier Academic Press, characterisation and management of these epidemics are challenging as native pathogens are often already wide- 3. Burgess TI, Wingfield MJ. Impact of fungi in natural forest eco- spread, and eradication is not viable. The next century will systems; a focus on Eucalyptus. In: Sivasithamparam K, Dixon likely see an unprecedented rise in forest pathogen epidem- KW, Barrett RL, editors. Microorganisms in plant conservation and biodiversity. Dordrecht: Kluwer Academic Publishers; 2002. ics, both native and alien; there is a need for a predictive p. 285–306. rather than a reactive response. Rather than focusing on ‘single pathogen-single host’ disease dynamics, a ‘whole 1 3 Current Forestry Reports (2022) 8:111–123 121 4. Burdon JJ, Thrall PH. Coevolution of plants and their pathogens 24. Paap T, Burgess TI, McComb JA, Shearer BL, Hardy GES. in natural habitats. Science. 2009;324:755–6. Quambalaria species, including Q. coyrecup sp. nov., impli- 5. Stenlid J, Oliva J. Phenotypic interactions between tree hosts and cated in canker and shoot blight diseases causing decline of invasive forest pathogens in the light of globalization and climate Corymbia species in the southwest of Western Australia. change. Philos Trans R Soc B Biol Sci. 2016;371:20150455. Mycol Res. 2008;112:57–69. 6. Anderson PK, Cunningham AA, Patel NG, Morales FJ, Epstein 25. Paap T, Burgess TI, Calver M, McComb J, Shearer B, Hardy PR, Daszak P. Emerging infectious diseases of plants: pathogen GES. A thirteen-year study on the progression of a severe can- pollution, climate change and agrotechnology drivers. Trends ker disease on the health of a keystone tree in a Mediterranean Ecol Evol. 2004;19:535–44. forest and woodland ecosystem. For Pathol. 2017;47:e12292. 7. Paap T, Wingfield MJ, Burgess TI, Wilson JRU, Richardson DM, 26. Ramalho CE, Laliberté E, Poot P, Hobbs RJ. Complex effects Santini A. Invasion frameworks: a forest pathogen perspective. of fragmentation on remnant woodland plant communi- Curr For Rep. 2022; 8:74–89 ties of a rapidly urbanizing biodiversity hotspot. Ecology. 8. Bonnamour A, Gippet JMW, Bertelsmeier C. Insect and plant 2014;95:2466–78. invasions follow two waves of globalisation. Ecol Lett. 2021. 27. Zambrano J, Garzon-Lopez CX, Yeager L, Fortunel C, Cordeiro https:// doi. org/ 10. 1111/ ele. 13863. NJ, Beckman NG. The effects of habitat loss and fragmentation 9. Rizzo DM, Garbelotto M. Sudden oak death: endangering on plant functional traits and functional diversity: what do we California and Oregon forest ecosystems. Front Ecol Environ. know so far? Oecologia. 2019;191:505–18. 2003;1:197–204. 28. Arroyo-Rodríguez V, Saldana-Vazquez RA, Fahrig L, Santos 10. Rigling D, Prospero S. Cryphonectria parasitica, the causal BA. Does forest fragmentation cause an increase in forest tem- agent of chestnut blight: invasion history, population biology perature? Ecol Res. 2017;32:81–8. and disease control. Mol Plant Pathol. 2018;19:7–20. 29. Latimer CE, Zuckerberg B. Forest fragmentation alters winter 11. Shearer BL, Crane CE, Barrett S, Cochrane A. Phytophthora cin- microclimates and microrefugia in human-modified landscapes. namomi invasion, a major threatening process to conservation of Ecography. 2017;40:158–70. flora diversity in the South-west Botanical Province of Western 30. Watson JEM, Evans T, Venter O, Williams B, Tulloch A, Stewart Australia. Aust J Bot. 2007;55:225–38. C, et al. The exceptional value of intact forest ecosystems. Nat 12. Brasier CM, Buck KW. Rapid evolutionary changes in a globally Ecol Evol. 2018;2:599–610. invading fungal pathogen (Dutch elm disease). Biol Invasions. 31.•• Paap T, Burgess TI, Rolo V, Steel E, Hardy GESJ. Anthropo- 2001;3:223–33. genic disturbance impacts stand structure and susceptibility 13. Pautasso M, Aas G, Queloz V, Holdenrieder O. European ash of an iconic tree species to an endemic canker pathogen. For (Fraxinus excelsior) dieback–a conservation biology challenge. Ecol Manag. 2018;425:145–53. Data driven paper based on Biol Cons. 2013;158:37–49. extensive surveys showing a clear evidence for anthropogenic 14.•• Desprez-Loustau M-L, Aguayo J, Dutech C, Hayden KJ, Hus- disturbance driving a tree decline. son C, Jakushkin B, et al. An evolutionary ecology perspective 32. Dawes W, Ali R, Varma S, Emelyanova I, Hodgson GA, McFar- to address forest pathology challenges of today and tomorrow. lane DJ. Modelling the effects of climate and land cover change Ann For Sci. 2016;73:45–67. An important review highlight- on groundwater recharge in southwest Western Australia. Hydrol ing the need to consider evolutionary ecology perspectives Earth Syst Sci. 2012;16:2709–22. in forest health research. The authors also provide policy 33. Matusick G, Ruthrof KX, Kala J, Brouwers NC, Breshears DD, recommendations and identify areas of research need. Hardy GES. Chronic historical drought legacy exacerbates 15. Burgess TI, Wingfield MJ. Pathogens on the move: a 100 tree mortality and crown dieback during acute heatwave-com- year global experiment with planted eucalypts. Bioscience. pounded drought. Environ Res Lett. 2018;13:095002. 2017;67:14–25. 34. Ruthrof KX, Breshears DD, Fontaine JB, Froend RH, Matusick 16.•• Ghelardini L, Pepori AL, Luchi N, Capretti P, Santini A. Driv- G, Kala J, et al. Subcontinental heat wave triggers terrestrial and ers of emerging fungal diseases of forest trees. For Ecol Manag. marine, multi-taxa responses. Sci Rep. 2018;8:1–9. 2016;381:235–46. Provides an overview of host-pathogen- 35.• Sapsford SJ, Paap T, Hardy GESJ, Burgess TI. Anthropogenic environment relationships with emphasis on interactions disturbance impacts mycorrhizal communities and abiotic soil among anthropogenic disturbance, new and emerging fungi properties: implications for an endemic forest disease. Front For (i.e. invasive species, new strains, new hybrids and latent Glob Chang. 2021;3:e593243. Strong empirical evidence for pathogens) and potential range shifts of fungi. the complex interactions between tree decline and soil biota. 17. Hepting GH. Climate and forest diseases. Annu Rev Phytopathol. 36. Guo Q, Riitters KH, Potter KM. A subcontinental analysis of for- 1963;1:31–50. est fragmentation effects on insect and disease invasion. Forests. 18. Hennon PE, Frankel SJ, Woods AJ, Worrall JJ, Norlander D, 2018;9:744. Zambino PJ, et al. A framework to evaluate climate effects on 37. Burgess TI, Scott JK, McDougall KL, Stukely MJC, Crane C, forest tree diseases. For Pathol. 2020;50:e12649. Dunstan WA, et al. Current and projected global distribution of 19. Sinclair WA. Comparisons of recent declines of white ash, Phytophthora cinnamomi, one of the world’s worst plant patho- oaks, and sugar maple in northeastern woodlands. Cornell gens. Glob Change Biol. 2017;23:1661–74. Plantations. 1965;20:62–7. 38. Paap T, Brouwers N, Burgess TI, Hardy GES. Importance of 20. Manion PD. Tree disease concepts. New Jersey: Prentice-Hall; climate, anthropogenic disturbance and pathogens (Quamba- 1981. laria coyrecup and Phytophthora spp.) on marri (Corymbia 21. Manion PD. Tree disease concepts. Englewood Cliffs: Prentice calophylla) tree health in southwest Western Australia. Ann For Hall; 1991. Sci. 2017;74:62. 22. Holdenrieder O, Pautasso M, Weiberg PJ, Lonsdale D. Tree 39. Croeser L, Admiraal R, Barber PA, Burgess TI, Hardy GESJ. diseases and landscape processes: the challenge of landscape Reflectance spectroscopy to characterise the response of Corym - pathology. Trends Ecol Evol. 2004;19:446–52. bia calophylla to Phytophthora root rot and waterlogging stress. 23. Desprez-Loustau M-L, Marçais B, Nageleisen LM, Piou D, Forestry. 2021. https:// doi. org/ 10. 1093/ fores try/ cpab0 45. 40. Corcobado T, Vivas M, Moreno G, Solla A. Ectomycorrhizal Vannini A. Interactive effects of drought and pathogens in symbiosis in declining and non-declining Quercus ilex trees forest trees. Ann For Sci. 2006;63:597–612. 1 3 122 Current Forestry Reports (2022) 8:111–123 infected with or free of Phytophthora cinnamomi. For Ecol Man- New England and linking disease incidence with tree size, age. 2014;324:72–80. stand density and soil type. 41. Ennos RA. Resilience of forests to pathogens: an evolutionary 59.•• Schulz AN, Mech AM, Asaro C, Coyle DR, Cram MM, ecology perspective. Forestry. 2015;88:41–52. Lucardi RD, et al. Assessment of abiotic and biotic factors 42. Hossain M, Veneklaas EJ, Hardy GESJ, Poot P. Tree host–patho- associated with eastern white pine (Pinus strobus L.) dieback gen interactions as influenced by drought timing: linking physi- in the Southern Appalachian Mountains. For Ecol Manag. ological performance, biochemical defence and disease severity. 2018;423:59–69. This paper considers numerous biotic and Tree Physiol. 2019;39:6–18. abiotic factors driving the landscape level impacts of white 43. Camarero JJ, Bigler C, Linares JC, Gil-Pelegrín E. Synergistic pine dieback. effects of past historical logging and drought on the decline of 60. Livingston WH, Kenefic LS. Low densities in white pine Pyrenean silver fir forests. For Ecol Manage. 2011;262:759–69. stands reduce risk of drought-incited decline. For Ecol Manage. 44. Oliva J, Colinas C. Canopy openings may prevent fir broom rust 2018;423:84–93. (Melampsorella caryophyllacearum) infections. Eur J For Res. 61. Costanza KKL, Whitney TD, McIntire CD, Livingston WH, 2007;126:507–11. Gandhi KJK. A synthesis of emerging health issues of eastern 45.•• Oliva J, Colinas C. Decline of silver fir (Abies alba Mill.) stands white pine (Pinus strobus) in eastern North America. For Ecol in the Spanish Pyrenees: role of management, historic dynamics Manage. 2018;423:3–17. and pathogens. For Ecol Manag. 2007;252:84–97. Good exam- 62. Costanza KKL, Crandall MS, Rice RW, Livingston WH, Munck ple of how to try to understand forest decline at a large scale IA, Lombard K. Economic implications of a native tree dis- by sampling stands at random and trying to link poor health ease, Caliciopsis canker, on the white pine (Pinus strobus) lum- with different pathogens. ber industry in the northeastern United States. Can J For Res. 46. Johannesson H, Stenlid J. Molecular identification of wood- 2019;49:521–30. inhabiting fungi in an unmanaged Picea abies forest in Sweden. 63. Hayhoe K, Wake CP, Huntington TG, Luo L, Schwartz For Ecol Manage. 1999;115:203–11. MD, Sheffield J, et  al. Past and future changes in climate 47. Oliva J, Colinas C. Epidemiology of Heterobasidion abietinum and hydrological indicators in the US Northeast. Clim Dyn. and Viscum album on silver fir (Abies alba) stands of the Pyr - 2007;28:381–407. enees. For Pathol. 2010;40:19–32. 64. Hayhoe K, VanDorn J, Croley T II, Schlegal N, Wuebbles D. 48. Oliva J, Suz LM, Colinas C. Ecology of Armillaria species on Regional climate change projections for Chicago and the US silver fir (Abies alba) in the Spanish Pyrenees. Ann For Sci. Great Lakes. J Great Lakes Res. 2010;36:7–21. 2009;66:603. 65.•• Simler-Williamson AB, Rizzo DM, Cobb RC. Interacting effects 49.•• Sangüesa-Barreda G, Camarero JJ, Oliva J, Montes F, Gazol of global change on forest pest and pathogen dynamics. Ann Rev A. Past logging, drought and pathogens interact and contribute Ecol Evol Syst. 2019;50:381–403. Review paper summariz- to forest dieback. Agric For Meteorol. 2015;208:85–94. Shows ing the interactions between tree mortality, pathogens, pests, how declining trees were mostly dominant or co-dominant the environment and climate change. The authors develop trees that were released after selective cuttings. a framework to explain how diverse global change drivers 50. Améztegui A, Brotons L, Coll L. Land-use changes as major impact the disease triangle. drivers of mountain pine (Pinus uncinata Ram) expansion in the 66. Wyka SA, Smith C, Munck IA, Rock BN, Ziniti BL, Broders Pyrenees. Glob Ecol Biogeogr. 2010;19:632–41. K. Emergence of white pine needle damage in the north- 51. Slippers B, Hurley BP, Wingfield MJ. Sirex woodwasp: a model eastern United States is associated with changes in pathogen for evolving management paradigms of invasive forest pests. pressure in response to climate change. Glob Change Biol. Annu Rev Entomol. 2015;60:601–19. 2017;23:394–405. 52. Camarero JJ, Gazol A, Sangüesa-Barreda G, Oliva J, Vicente- 67. Munck IA, Luther T, Wyka S, Keirstead D, McCracken K, Serrano SM. To die or not to die: early warnings of tree dieback Ostrofsky WD, et al. Soil and stocking effects on Caliciopsis in response to a severe drought. J Ecol. 2015;103:44–57. canker of Pinus strobus L. Forests. 2016;7:269. 53. Macias M, Andreu L, Bosch O, Camarero JJ, Gutiérrez E. 68.• Costanza KKL, Livingston WH, Fraver S, Munck IA. Dendro- Increasing aridity is enhancing silver fir (Abies alba mill.) chronological analyses and whole-tree dissections reveal Cali- water stress in its south-western distribution limit. Clim Chang. ciopsis canker (Caliciopsis pinea) damage associated with the 2006;79:289–313. declining growth and climatic stressors of eastern White Pine 54. Gazol A, Camarero JJ, Gutiérrez E, Popa I, Andreu-Hayles L, (Pinus strobus). Forests. 2020;11:347. Paper that used den- Motta R, et al. Distinct effects of climate warming on popu - drochronology and whole-tree dissection to link a decrease in lations of silver fir (Abies alba) across Europe. J Biogeogr. tree growth to tree damage, i.e. cankers with abiotic stressors 2015;42:1150–62. (weather events—droughts and a hurricane). 55. Marqués L, Peltier DMP, Camarero JJ, MlA Zavala, Madrigal- 69. Whitney TD, Cram MM, Barnes BF, Yao J, Lucardi RD, Gandhi González J, Sangüesa-Barreda G, et al. Disentangling the lega- KJK. Tree-level distribution of a novel insect-pathogen complex cies of climate and management on tree growth. Ecosystems. and its potential contribution to eastern white pine dieback. For 2021. https:// doi. org/ 10. 1007/ s10021- 021- 00650-8. Ecol Manage. 2018;423:49–58. 56. Peck C. Annual report on the New York State Museum of 70. Mech AM, Asaro C, Cram MM, Coyle DR, Gullan PJ, Cook Natural History. Report of the botanist. Albany, Regents of LG, et al. Matsucoccus macrocicatrices (Hemiptera: Matsucoc- the University of the State of New York. 1980. Available at: cidae): first report, distribution, and association with sympto- https:// www. biodi versi tylib rary. org/ item/ 110212. matic eastern white pine in the southeastern United States. J 57. Fitzpatrick HM. Monograph of the Coryneliaceae. Mycologia. Econ Entomol. 2013;106:2391–8. 1920;12:206–37. 71. Broders K, Munck I, Wyka S, Iriarte G, Beaudoin E. Charac- 58.•• Munck IA, Livingston WH, Lombard K, Luther T, Ostrofsky terization of fungal pathogens associated with white pine nee- WD, Weimer J, et al. Extent and severity of Caliciopsis canker dle damage (WPND) in northeastern North America. Forests. in New England, USA: an emerging disease of eastern white 2015;6:4088–104. pine (Pinus strobus L.). Forests. 2015;6:4360–73. One of the 72. Livingston WH, Munck I, Lombard K, Weimer J, Bergdahl first papers describing the extent of Caliciopsis canker in A, Kenefic LS et  al. MP764: Field Manual for Managing 1 3 Current Forestry Reports (2022) 8:111–123 123 Eastern White Pine Health in New England. Maine Agricul- endangered monkey puzzle tree (Araucaria araucana) in Chile. tural and Forest Experiment Station Miscellaneous Publications. Biol Cons. 2012;152:110–8. 2019. https://digit alc ommons. libr ar y.umaine. edu/ aes_ miscp ubs/ 82. Shepherd JD, Ditgen RS. Human use and small mammal com- 24 munities of Araucaria forests in Neuquén, Argentina. Mastozo- 73. Vélez ML, Marfetán JA, Salgado Salomon ME, Taccari LE. ología Neotropical. 2005;12:217–26. Mortierella species from declining Araucaria araucana trees in 83. Cóbar-Carranza AJ, García RA, Pauchard A, Pena E. Effect of Patagonia Argentina. For Pathol. 2020;50:e12591. Pinus contorta invasion on forest fuel properties and its poten- 74. Balocchi F, Wingfield MJ, Ahumada R, Barnes I. Pewenomy - tial implications on the fire regime of Araucaria araucana and ces kutranfy gen. nov. et sp. nov. causal agent of an important Nothofagus antarctica forests. Biol Invasions. 2014;16:2273–91. canker disease on Araucaria araucana in Chile. Plant Pathol. 84. Molina JR, Martin A, Drake F, Martín LM, Herrera MÁ. Frag- 2021;70:1243–59. mentation of Araucaria araucana forests in Chile: quantification 75. Vélez ML, Salgado Salomón ME, Marfetan A, Tirante SI, Mattes and correlation with structural variables. iForest-Biogeosci For. Fernández H, Avila M, Caracterización desecación del dosel y 2015;9:244. sanidad de Araucaria araucana en Argentina. Technical Report. 85. Dash JP, Watt MS, Pearse GD, Heaphy M, Dungey HS. Assess- 2018. Available from: https:// doi. org/ 10. 13140/ RG.2. 2. 14227. ing very high resolution UAV imagery for monitoring forest 78889. health during a simulated disease outbreak. ISPRS J Photo- 76. Garreaud RD, Boisier JP, Rondanelli R, Montecinos A, gramm Remote Sens. 2017;131:1–14. Sepúlveda HH, Veloso-Aguila D. The central Chile mega 86. Dakin N, White D, Hardy GES, Burgess TI. The opportunis- drought (2010–2018): a climate dynamics perspective. Int J tic pathogen, Neofusicoccum australe, is responsible for crown Climatol. 2020;40:421–39. dieback of peppermint (Agonis flexuosa) in Western Australia. 77. Cordero RR, Asencio V, Feron S, Damiani A, Llanillo PJ, Australas Plant Pathol. 2010;39:202–6. Sepulveda E, et al. Dry-season snow cover losses in the Andes 87. Dutech C, Barrès B, Bridier J, Robin C, Milgroom MG, Ravigné (18°–40° S) driven by changes in large-scale climate modes. Sci V. The chestnut blight fungus world tour: successive introduction Rep. 2019;9:1–10. events from diverse origins in an invasive plant fungal pathogen. 78.• Moreno-Gonzalez R, Giesecke T, Fontana SL. The impact of Mol Ecol. 2012;21:3931–46. recent land-use change in the Araucaria araucana forest in 88. McDonald BA, Linde C. Pathogen population genetics, evolu- northern Patagonia. Holocene. 2020;30:1101–14. Holistic study tionary potential and durable resistance. Annu Rev Phytopathol. of different types of impacts and how they effect a forest. 2002;40:349–79. 79. Mundo IA, Kitzberger T, Juñent FAR, Villalba R, Bar- 89. Paap T, Wingfield MJ, Burgess TI, Hulbert JM, Santini A. Har - rera MD. Fire history in the Araucaria araucana forests of monising the fields of invasion science and forest pathology. Argentina: human and climate influences. Int J Wildland Fire. NeoBiota. 2020;62:301–32. 2012;22:194–206. 80. Aagesen DL. Indigenous resource rights and conservation of Publisher's Note Springer Nature remains neutral with regard to the monkey-puzzle tree (Araucaria araucana, Araucariaceae): jurisdictional claims in published maps and institutional affiliations. a case study from southern Chile. Econ Bot. 1998;52:146–60. 81. Zamorano-Elgueta C, Cayuela L, González-Espinosa M, Lara A, Parra-Vázquez MR. Impacts of cattle on the South Ameri- can temperate forests: challenges for the conservation of the 1 3 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Current Forestry Reports Springer Journals

Anthropogenic Disturbances and the Emergence of Native Diseases: a Threat to Forest Health

Download PDF
13 pages

Loading next page...
 
/lp/springer-journals/anthropogenic-disturbances-and-the-emergence-of-native-diseases-a-tR0sSUdHWY

References (94)

Publisher
Springer Journals
Copyright
Copyright © Crown 2022
eISSN
2198-6436
DOI
10.1007/s40725-022-00163-0
Publisher site
See Article on Publisher Site

Abstract

Purpose of Review Human-caused global change is fundamentally altering natural forest ecosystems. More trees are exhibit- ing a wide range of symptoms indicative of poor vigour, particularly stressed species at the edge of their native ranges and stands growing on marginal sites. This review will focus on complex tree diseases (declines) caused by native pathogens and the key environmental drivers that contribute to this phenomenon. These systems are frequently complex, with multiple drivers at work. Recent Findings Using four cases studies on different continents, we explored the direct and indirect environmental drivers underlying these decline syndromes. Although climate and weather events seem to be usually associated with forest decline, we found that environmental disturbance by either forest management or land-use changes is also a global predisposing factor of decline which deserves more attention. Changes in land use have directly benefited pathogens such as root rots in the Pyrenees (Spain) or indirectly by making the environment more conducive for canker and foliar diseases in Australia and the USA. Focus on land-use changes could improve understanding of current decline problems such as those affecting Araucaria in Chile. Summary The next century will almost certainly see an unprecedented rise in forest pathogen epidemics, requiring a proac- tive rather than reactive response. Diseases caused by native pathogens with complex aetiologies will become more common, and recognising, characterising and managing these epidemics are difficult because native pathogens are frequently already widespread, and eradication is not feasible. We need to start approaching these issues from a ‘whole ecosystem’ perspective, highlighting the many aspects and entanglements of forest declines and allowing us to respond with management options tailored to each scenario. The approach proposed here provides logical steps based on six questions to untangle the direct and indirect environmental drivers of tree declines. Keywords Abies alba · Araucaria araucana · Corymbia calophylla · Global change · Pinus strobus · Tree decline This article is part of the Topical Collection on Forest Pathology * Treena I. Burgess School of Biological Sciences, University of Canterbury, t.burgess@murdoch.edu.au Christchurch 8041, New Zealand Department of Plant, Soil and Microbial Sciences Harry Butler Institute, Murdoch University, Murdoch 6150, and the Department of Forestry, Michigan State University, Australia East Lansing, MI 48824, USA Forestry and Agricultural Biotechnology Institute Forestry and Agricultural Biotechnology Institute, Department of Plant and Soil Sciences, University Department of Biochemistry, Genetics and Microbiology, of Pretoria, 0002 Pretoria, South Africa University of Pretoria, 0002 Pretoria, South Africa Deparment of Crop and Forest Sciences, University of Lleida, 25198 Lleida, Spain Joint Research Unit CTFC-AGROTECNIO-CERCA Center, 25198 Lleida, Spain Vol.:(0123456789) 1 3 112 Current Forestry Reports (2022) 8:111–123 barriers are crossed. There are numerous examples of this: Introduction sudden oak death in the western USA [9], chestnut blight [10], Phytophthora dieback in the southwest of Australia Forest systems are experiencing unprecedented transforma- [11], Dutch elm disease [12] and Ash dieback [13]. tion rates due to many disruptions related to global change, Pertinent to this review, native pathogens do not need to including land clearing and fragmentation, severe droughts overcome geographical or evolutionary boundaries. How- and wildfires and outbreaks of invasive alien pests and ever, the environmental barrier may be overcome due to pathogens [1]. Several reviews have explored these topics. land-use change and/or overarching climate change, lead- However, one gap in the current literature is exploring how ing to situations where native pathogens exhibit increased anthropogenic disturbances lead to the emergence of native pathogenicity to co-evolved hosts. For example, selective pathogens resulting in disease epidemics more typical of logging or clear-felling coups can result in an even-aged invasive alien pathogens. Understanding and teasing out monoculture of a native tree species that is now equally sus- the drivers of native epidemics in forest ecosystems will •• ceptible to specific pathogens [14 , 15]. The environment aid in mitigating this problem. As eradicating ubiquitous can alter host–pathogen relationships, and depending on the native pathogens is not an option, management strategies region, climatic conditions may become more or less favour- must focus on ameliorating ecosystem stress, a complex able for pathogens. Weather (short-term atmospheric con- undertaking. ditions) and climate (weather of a specific region averaged Disease is a consequence of a virulent pathogen, a suscep- over a long time period) both impact pathogens, their hosts tible host and a conducive environment (i.e. the disease tri- and their interactions. Climate change refers to long-term angle [2]). Trees in natural ecosystems are mixed in age and changes in climate. For example, climate change leading species composition, and the impact of pathogens adapted to to long-term drying is a chronic change while drought is a particular host or life stage is limited by the availability of an acute change; both may favour pathogens by enhancing resources [3]. Natural ecosystems are, typically, in balance their fitness or driving expansion in distribution ranges and/ with their native pathogens, and severe disease outbreaks or exerting stress on tree hosts, predisposing them to disease are rare [4]. However, this co-evolution occurred over time •• development [16 ]. and within an environmental envelope [5]. Human activities Perhaps, the first to highlight the role of climate in forest have disturbed this natural balance between trees and their disease was Hepting [17], who concluded that a severe out- co-evolved pathogens, reducing ecosystem resilience. These break of a native pathogen ‘is a rare removal by the weather of activities include land clearing and fragmentation, leading obstacles that ordinarily constrain the pathogen’. In an era of to more edges exposed to climatic fluctuations and other global change, the disease triangle must be updated to consider stressors such as increased run-off or pesticides from agri- the environmental component in two timeframes: the weather, culture. Harvesting of trees, selective or clear-felling, alters which must be conducive to disease development, and overall age class and species composition, and hence the availability climate change and the underlying stress it causes [18]. The of susceptible hosts. This complex interplay between natural disease triangle only explains the point at which disease is ini- resilience and increased stressors can lead to native patho- tiated and the subsequent symptoms that develop (acute); other gens causing disease epidemics as impactful as those typi- models (such as Manion’s decline spiral) treat tree disease in cally seen for invasive pathogens. In addition to these direct a more holistic space taking into account other interactions of impacts by human activities, the impacts of anthropogenic the host and pathogens. The concept of chronic tree disease or climate change are increasingly experienced in forest sys- tree decline caused by interchangeable predisposing, inciting tems, with this further contributing to disease development and contributing factors was first proposed by Sinclair [19]. by native pathogens. Manion [20] developed this concept further and proposed the The study of emerging infectious diseases has its his- tree disease spiral and later the decline disease spiral [21]. The tory in medical and veterinary fields but has also applied to early 2000s saw a rise in studies and reviews of challenges to plant pathogens [6]. Three barriers limit the development of forest health in the face of globalisation and climate change [6, emerging infectious diseases: geographical, environmental 22, 23]. Drought, in particular, was seen as a significant driver and evolutionary (compatibility) (for detail, see Paap et al. of disease emergence. [7]). Release from any of these barriers can result in disease The impact of invasive alien forest pathogens is well development. In the context of invasive alien pathogens, documented; this review will concentrate on complex tree globalisation (trade leading to accidental movement of for- diseases (declines) caused by native pathogens in the era of est pathogens to naïve suitable hosts) allows pathogens to anthropogenic global change. As elucidated by three case overcome geographical barriers [8]. If this leads to oppor- studies, we explore the key environmental drivers behind tunities for microorganisms to encounter naïve hosts lacking this phenomenon, showing that these systems are often co-evolved resistance, then the evolutionary/compatibility complex, with multiple drivers involved. Finally, using 1 3 Current Forestry Reports (2022) 8:111–123 113 Fig. 1 Quambalaria coyrecup causing cankers on Corymbia calophylla. Left, leading to branch dieback and death of roadside trees; centre, extensive perennial cankers; right, sporulation of Q. coyrecup on the canker surface the decline of Araucaria araucana in South America as [26]. This habitat loss has resulted in forest fragments inter- an example, we recommend an experimental approach that spersed amongst various land-use types [27]. Forest fragments could be applied to understand the dynamics of emerging have distinct edge habitats that experience different envi- forest pathogen outbreaks. We highlight the need for this ronmental conditions compared to the interior of fragments approach to consider both temporal and multi-spatial scales. [28–30]. Specifically, highly fragmented areas in SWWA have resulted in remnant tree stands dominated by C. calophylla, and these fragmented areas are surrounded by die ff rent types of land Marri Canker; Pathogen: Quambalaria use (e.g. road and land used for horticulture, agriculture, viti- coyrecup, Host: Corymbia calophylla culture or grazing). It is in these highly fragmented areas that canker incidence is highest. Forest edges only exposed to one Aetiology and Extent type of land use, and interiors of forest fragments have lower •• canker incidence than highly fragmented areas [31 ]. Quambalaria coyrecup is a basidiomycete smut-like fungus The SWWA has experienced dramatic climate changes. thought to be endemic to the southwest of Western Australia Rainfall has declined over the past 30 years, and in com- (SWWA), and it is the causative agent of stem cankers in Cor- bination with a growing population requiring increases in ymbia calophylla, a keystone Myrtaceae tree species endemic water demand, groundwater levels have declined [32]. The to SWWA [24]. Excessive bleeding (gummosis), staining region has also experienced heatwave-compounded drought limbs or trunks dark red, splitting and eventual shedding of events [33]. With both long-term precipitation reduction bark revealing perennial cankers and Q. coyrecup sporula- and drought, SWWA has experienced long-term drying, the tion as powdery white masses within the cankered area are impacts of which have already been observed in crown die- all symptoms of this disease [25]. As cankers progress, they back in dominant forest species, Eucalyptus marginata and eventually ‘girdle’ the affected limb or trunk, resulting in the C. calophylla [34]. This overall climate change is one of the death of the limb or death of the entire tree (Fig. 1). These abiotic factors driving canker incidence in C. calophylla. symptoms were first observed in C. calophylla in 1939–1940, but at the time were of no serious concern. In subsequent dec- Indirect Environmental Drivers ades, additional biotic and abiotic factors have caused changes in this native pathogen-host relationship. Such factors include Anthropogenic disturbance also changes soil microclimate, climate change, increases in habitat fragmentation and interac- which results in alterations in soil chemistry and compo- tions with invasive plant pathogens. By the 1990s, these stem • sition belowground [35 ] and plant diversity aboveground cankers were causing a noticeable decline of C. calophylla. •• [31 ]. Belowground processes and communities are highly sensitive to these changes, further predisposing C. calo- Environmental Drivers phylla to canker disease. For example, concentrations of key soil nutrients (i.e. nitrogen, phosphorus and potassium) are The SWWA is a highly fragmented landscape with increasing much higher along edge habitats where C. calophylla has a pressure from expansion in both agriculture and urbanisation • higher canker incidence [35 ]. In addition, communities of 1 3 114 Current Forestry Reports (2022) 8:111–123 Fig. 2 (Left) Decline of silver fir (Abies alba) in the Pyrenees. (Centre) Leading to defoliation and tree mortality. (Right) Mortality is associated with a widespread presence of root rots such as Heterobasidion abietinum amongst other pathogens beneficial mycorrhizal fungi have lower richness and diver - timing and length of droughts within these environments are sity in edge habitats in comparison to forest habitats [35 ]. also important in disease development [42]. Fragmented forests can experience greater pressure from invasive plant pathogens [36]. Phytophthora spp. Summary have caused devastation to forests in SWWA, especially the invasive Phytophthora cinnamomi [37]. Landscape- Overall, the decline of C. calophylla seems to have been scale surveys identified that C. calophylla present on sites instigated by anthropogenic disturbance but is a complicated infested with pathogenic Phytophthora species had higher decline involving changes both above- and belowground. levels of canker incidence [38]. Glasshouse studies also Specifically, a drying climate combined with habitat frag- showed C. calophylla co-infected with Phytophthora spp. mentation and the indirect effects of habitat fragmenta- and Q. coyrecup were more stressed than C. calophylla tion (i.e. changes in soil nutrients and biotic communities) infected with Q. coyrecup only [39]. To add to the com- predisposes C. calophylla to canker disease caused by Q. plexity, the loss of ectomycorrhizal fungal diversity could coyrecup. play a role in Phytophthora spp. infection [40]. Together, these changes in abiotic and biotic characteristics of the soil are highly correlated with increased disease incidence Silver Fir Decline; Pathogens: Various, Host: in C. calophylla [35 ]. Abies alba Aboveground, anthropogenic disturbance has altered for- est stand structure where highly fragmented areas have dif- Aetiology and Extent ferent overstory composition than the interior of forest frag- •• ments [31 ]. Interior forest fragments consist of mixed E. The health of silver fir (Abies alba) in the Pyrenees (moun- marginata and C. calophylla overstory; E. marginata may be tain range straddling the border of France and Spain) has less tolerant to fragmentation as this species is not present in been of concern for the last three decades (Fig. 2). Several highly fragmented areas (however, E. marginata is removed stands in the southern side of the Pyrenees started showing by selective logging practices). In either case, the loss of signs of decline associated with the severe droughts occur- diversity in highly fragmented areas may have led to levels ring in the 1980s [43]. A large-scale pathological system- of pathogen pressure of Q. coyrecup above those which C. atic sampling revealed a high incidence of root rots such as calophylla is adapted to in their natural forest setting [41]. Heterobasidion annosum (42% of the stands) and Armil- The impacts of anthropogenic disturbance on C. calophylla laria spp. (93%), canker pathogens such as Melampsorella health can also interact with climate and drought events. Cli- caryophyllacearum (55% of the stands) or parasitic plants •• mate plays a major role in the development of cankers in C. such as Viscum album [44, 45 ]. At a Pyrenean scale, the calophylla. For example, cankers have been observed across parasitic plant Viscum album was the biotic agent most •• most of the range of C. calophylla, but areas with wetter and clearly associated with symptoms of decline [45 ]. Con- cooler climates have high incidences of canker [38]. The cerning the root rots, there is no information on the severity 1 3 Current Forestry Reports (2022) 8:111–123 115 of those pathogens and how much they increased in associa- been subjected to major shifts in temperature and precipita- tion with the decline process; however, the observed inci- tion, leading to increased drought and the decline of different dences (> 40%) are far greater than those observed in natural species. Silver fir in the Pyrenees has experienced a series of forests [46]. Later work on specific pathogens showed that droughts [53], much more severe than in other populations both H. annosum s.s. and H. abietinum affected fir stands, in the Alps or Romania [54]. although the latter was far more abundant [47]. Several spe- cies of Armillaria were also found affecting fir forests, with Indirect Environmental Drivers A. ceptistipes being the most abundant and the one associ- ated with higher defoliation. Aggressive Armillaria species Drought alone could not explain the phenomenon of decline such as A. ostoyae or A. gallica were more associated with and it was clear that it involved the effect of previous manage- fir-accompanying species such as Pinus uncinata or Fagus ment. Declining stands showed many more growth releases sylvatica than with fir decline [48]. than non-declining stands [43]. Management did not affect Later studies in more localised declining stands revealed all species similarly, and some species growing near silver fir high local severities of pathogens such as Amylostereum stands, such as Pinus sylvestris, benefited from it [55]. chailletii and Trichaptum abietinum, together with the Another critical aspect is the selection of trees to remain •• above-mentioned root rots [49 ]. Some interactions after logging. Trees showing symptoms of decline in the between the identified pathogens were found. For instance, 1980s were those growing slower at the beginning of the V. album was more prevalent in forests attacked by H. abi- century and before harvesting in the second half of the •• etinum [47]. Other secondary pests such as bark beetles from century [49 ]. Harvesting extracted the best and most vig- the genus Pityokteines have been associated with mortality orous trees and left those suppressed or co-dominant, prob- •• in declining forests [45 ]. ably with less capacity to adapt to the increased density and competition with the new cohort for the scarce water •• Environmental Drivers supplies [45 ]. Management triggered structural changes that contributed to forest decline appearing decades after. Fir forests were subjected to major logging during the sec- ond half of the twentieth century. During the selective log- ging process, some trees were left, and this caused massive Summary regeneration underneath. Thereafter, most of the fir stands remained untouched, and encroachment and competition Evidence shows that logging was the predisposing fac- were paramount. Thus, the most common forest structure tor for the decline of silver fir in the Pyrenees. Logging •• comprises two cohorts [45 ], with trees belonging to the during the second half of the twentieth century favoured older cohort showing the most symptoms of decline. In most root rot pathogens and dramatically changed the structure cases, the current land use involves a lower anthropogenic of the forest, leaving the weaker trees remaining in the pressure than in the past, allowing the forest to expand to stands. After harvesting, forest management mainly was areas previously used as grassland or crop areas [50]. Across stopped, and encroachment and high tree-to-tree competi- the Pyrenees, the abundance of Armillaria and Heteroba- tion caused stress to the remaining trees. Amongst those, sidion in dead trees and stumps and the abundance of Armil- decline affected co-dominant and suppressed trees left from laria in soil were associated with higher intensity logging the previous rotation. The droughts in the late 1980s were [47, 48]. The current prevalence of Heterobasidion is pos- an inciting factor for the decline, and it was then when the sibly inherited from the previous land use as no stump pro- crown condition of fir started deteriorating. Since then, mor - tection methods such as urea, Phlebiopsis gigantea or borate tality has affected the largest trees, where secondary pests were applied at that time. Viscum album showed a similar and pathogens contribute to tree death. association with former management practices, more preva- lent on those isolated trees with large diameter and opened crowns [47]. There is no information on the association of Amylostereum with forest fragmentation in the context of Caliciopsis Canker; Pathogen: Caliciopsis fir decline. However, it is known that wasps carrying the pinea, Host: Pinus strobus pathogen affect stressed trees [51]; therefore, the presence of the pathogen is probably associated with trees left after Aetiology and Extent the logging, the ones suffering the most considerable growth losses over the last century [52]. Pinus strobus (eastern white pine) will naturally regenerate The Pyrenean population of silver fir is the southernmost and tolerate a range of soil types and is utilised commer- distribution of the species in Eurasia. The Pyrenees have cially for lumber. Caliciopsis pinea is a canker pathogen 1 3 116 Current Forestry Reports (2022) 8:111–123 Fig. 3 Caliciopsis canker symptoms on Pinus strobus (eastern white cankers more evident when the bark is removed (photo credit centre pine): left, reddish flagging branches; centre, resinosis indicative of and right, James Jacobs, USFS) numerous cankers; right, numerous, small and sometimes cracking of P. strobus native to North America, with fruiting bodies Caliciopsis canker, and the disease has been associated with of C. pinea first reported in New York in 1880 [56]. Subse- regeneration (seedlings and saplings), pole timber mortality •• quently, Caliciopsis canker disease was reported as a ‘minor’ and sawtimber degradation [58 , 62]. canker disease with a ubiquitous distribution throughout the Seasonal projections forecast warmer, wetter springs and range of P. strobus [57]. Reports of Caliciopsis canker on winters coupled with dryer, hotter summers [63, 64]. Col- P. strobus have increased in severity and distribution in the lectively, these climate changes lead to conditions favourable last 20 years, particularly in the northeastern USA (New to pathogen reproduction and dissemination in the spring, England) and southeastern USA (the Southern Appalachian improved overwintering survival of pathogens and increased •• •• •• Mountains) [58 , 59 ], where regeneration and plant- water stress in the host during the summer [65 ]. Increased ing strategies have led to dense stands of P. strobus. The temperature and precipitation has been linked to the emer- disease is characterised by excessive resin production and gence of needle cast pathogens [66], and increased tempera- reddish sunken cankers on stems and branches as well as tures have been linked to increased severity of Caliciopsis •• •• bark fissures, crown thinning and dieback (Fig.  3) [58 ]. canker disease [59 ]. Serious canker disease and declining P. strobus have now been observed in the Great Lakes region of Michigan and Indirect Environmental Drivers Wisconsin, and recent surveys (2018–2019) have high- lighted the extensive distribution of the disease in these Pinus strobus is widely distributed across eastern America states. Caliciopsis pinea is a threat to P. strobus throughout on many soil types. Disease severity and incidence have not its native range, and the risk it poses to other hosts remains been associated with ecoregions, plant hardiness zones, slope •• •• •• unquantified [58 ]. or aspect [58 , 59 ]. Compared to well-drained, more fer- tile soils, disease incidence increased on sites with exces- Environmental Drivers sively or poorly drained soils, and disease severity increased •• on sites with nutrient-poor, excessively drained soils [58 ]. Management decisions facilitating the growth of P. strobus Disease incidence and severity were also higher in drier and on poor quality sites combined with a subsequent lack of shallow soils when compared to loamy soils [67]. management resulting in dense even-aged stands have led Costanza et al. [68 ] uncovered regional synchrony in to favourable conditions for the emergence of the native the timing of canker incidence and severity across different C. pinea. More specifically, replanting and regenerating P. sites; tree declines triggered by climate stress events (i.e. strobus on logged and abandoned agricultural and pasto- drought and flooding) occurred 1–3 years before canker ral land, coupled with a lack of management and fire sup- development. Disease severity is also positively associ- •• pression, has led to overstocked, even-aged stands on com- ated with mean annual temperature [59 ]. Climate change pacted and plough pan soils that restrict root penetration likely has wide-ranging impacts across broad geographical [60, 61]. Together, these factors are driving the emergence regions, and local differences in incidence and severity of C. pinea. All age classes of P. strobus can be impacted by may be exacerbated by poor site and stand conditions. 1 3 Current Forestry Reports (2022) 8:111–123 117 Other biological pests and pathogens such as a native scale Araucaria Decline: an Emerging Disease insect and a complex of native foliar fungi are thought to com- of Natural Forests in South America pound climate, stand and site stresses. The herbivorous insect Matsucoccus macrocicatrices pierces P. strobus bark and feeds A newly documented decline of Araucaria araucana on the sap, creating numerous wounds that are thought to add (Araucaria, Pewén or the Monkey Puzzle tree) emerged stress to the tree and facilitate the entry of C. pinea [69]. How- between 2015 and 2016 (Fig.  4). This tree species is ever, M. macrocicatrices has only recently been associated with endemic to the south-central Andes Mountain range slopes C. pinea cankers [69, 70] and was previously considered benign. in Chile and Argentina and the coastal range of Chile. Therefore, the association between Caliciopsis canker disease Field surveys undertaken inside its natural range at dif- and M. macrocicatrices is unclear. White pine needle pathogens ferent locations identified symptomatic trees in all visited (Lophophacidium dooksii, Lecanosticta acicola and Bifusella areas. A broad initial description of symptoms consistently linearis) are native foliar fungi that cause premature needle loss identified dieback of portions of the crown of trees with [71], with disease severity linked to warmer and wetter seasons the death of a small proportion of young trees (between [61, 66], with associated host mortality exacerbated by site and 1.5 and 3 m), and, in rare cases, death of full adult trees stand characteristics and the presence of Caliciopsis canker dis- [73, 74]. Knowledge of this new disease is still scarce, and ease [68 ]. the factors driving its emergence are not understood. Sur- veys at different sites (latitudes) across the Andes distribu- Summary tion have shown the most prevalent symptoms to be can- kers on branches and stems. These cankers slowly girdle Overstocking, deficient soil conditions (poor drainage, nutrient- healthy-looking branches and stems, causing the death of poor, shallow), pests and pathogens are linked with increased the affected organs. A fungus residing in a novel genus and Caliciopsis canker disease incidence and severity. Younger, species, Pewenomyces kutranfy, was found to be the causal smaller trees are more impacted than larger trees, and inad- agent of these cankers [74]. This pathogen is believed to equate soil water and excessively shallow-rooted trees are more be native as it has not been found elsewhere and is clearly likely to be impacted during drought events. In general, selecting adapted to the cold temperature characteristic of high-alti- sites with deep, sandy, well-drained soils and stand thinning at tude environments. While evidence suggests this fungal prescribed size classes is recommended to increase tree vigour, canker disease is the prevalent disease associated with the resilience and resource availability [72]. Caliciopsis canker has dieback observed in A. araucana in the Andes [74], sites now been observed in the Great Lakes region in Michigan and exist where cankers are only scarcely observed and where Wisconsin. Disease severity is currently lower than observed in other abiotic factors and biotic agents seem predominant the eastern states, and current research focuses on documenting [75]. The observation of both cankers and other symptoms the distribution, impact and epidemiology in the Great Lakes suggests that different disease syndromes may be present region. in different sites (populations). Fig. 4 Decline of Araucaria araucana in Chile: left, crown symptoms on adult trees; centre, dieback of branches associated with girdling can- kers; right, cankers on branches caused by Pewenomyces kutranfy 1 3 118 Current Forestry Reports (2022) 8:111–123 This decline may be driven by changes in weather, includ- Recommendations for an Experimental ing several years of intense drought [76], a rise in maximum Approach to Studying Emerging Native and minimum temperatures and a reduction in snow precipita- Diseases tion and persistence (also increasing drought in the following summer) [77]. Araucaria forests have a long history of anthro- Here, we detail the steps of an experimental approach pogenic disturbances, including an intensive reduction in for- (Fig. 5), with an outline to the approach rather than describ- est area since the arrival of Euro-American settlers through ing all the possible factors to be explored, as we believe intentional fires for clearing lands for grazing [78 , 79] and the outcome of each progressive step will guide the next intensive logging [80]. Most of the Araucaria forests were step. We encourage the inclusion of multidisciplinary teams, protected in the 1900s to ameliorate this reduction; however, encompassing at least forest pathologists, landscape ecolo- the disturbance has continued in parts of their distribution. gists, plant physiologists, soil scientists, climate modellers Overgrazing and cattle ranching [81], the introduction of alien and biostatisticians as deemed necessary, as efforts to under - mammals [82] and the increasing establishment of planta- stand and mitigate these declines require a detailed under- tion forests have further contributed to the fragmentation and standing of multiple factors and potential mitigation options. alteration of fire regimes [83, 84]. These disturbances have been shown to impact the health and regeneration capacity of Step 1. Is a single pathogen consistently associated the species. However, no large-scale studies have examined with the symptoms, or is there a more complex decline the link between these factors and tree health status. Conse- without a specific pathogen as a key component? quently, the potential importance of these factors as drivers of this recently emerged decline remains unknown. Studying Systematic surveys of symptomatic and asymptomatic trees a new decline such as this across a large area and in rugged should be undertaken at multiple locations to develop an under- terrain is challenging. Below, we develop an experimental standing of the disease aetiology, including disease progression, six-step approach to untangle the dynamics of complex tree and if a primary pathogen/s can be consistently observed or declines. not. The inclusion of specialists on different pathogens would increase the likelihood of correctly diagnosing the disease-caus- ing agent. The possibility of involvement of multiple pathogens, Fig. 5 An experimental approach to understanding a forest decline syndrome based on six key questions 1 3 Current Forestry Reports (2022) 8:111–123 119 the simultaneous emergence of disease syndromes and/or a gen- plot, canopy cover, sunlight penetration, slope, aspect, pH, eral underlying decline deserves careful consideration at this soil moisture). These variables can be used in linear model- initial stage. ling approaches to see which are significant in predicting In cases where a primary pathogen is found, answer- the health parameters of the populations. Surveys can be ing questions regarding its origin and biology may become conducted to determine disease incidence in sites experi- relevant, such as whether it is native or alien, or whether encing these disturbances or not (i.e. comparative study it has arisen through an evolutionary process (hosts jump, design). Surveys can include comparing damage inside/ host shift or host range expansion). Suppose a diversity of outside protected areas, comparing areas with contrasting secondary pathogens are detected. In that case, a stronger management histories (e. g. wood extraction, grazing, oth- emphasis should turn towards the host’s condition, looking ers; policy changes) and comparing sites where restoration at whether there are any evident localised abiotic drivers or programmes may have been implemented (e. g. planting, stressors, or if a broader range complex condition may be removing alien vegetation and animals). Alternatively, a underlying, i.e. Manion decline spiral. historical reconstruction of the forests (30–50–80 or longer years ago) can be included, combining information such as Step 2. Is this a local or large-scale problem? land-use changes, forest adaptation to human perturbation events or regimes still present or interrupted, and/or changes Systematic surveys should be undertaken at a larger in forests management. scale (ideally across the entire host range) to understand the scale of the issue. For example, is it occurring in a Step 4. Have there been changes in short- and/or long- single stand, multiple stands or across the entire distribu- term climate and/or weather conditions? tion range of the host? Assessing the consistency of symp- toms and pathogens needs to be considered by applying Climatic conditions can be considered at different tem- standardised and coordinated methods for disease charac- poral and spatial scales. Weather changes refer to short- terisation, scoring and sampling. Hyperspectral imaging term atmospheric conditions, while climate is the weather and other remote sensing tools could be considered [85]. of a specific region averaged over a long time. Historical Fungal population genetics studies can be used to assess (long-term) climate data for sites showing different levels if genotypes associated with disease differ from those in of disease/damage can provide evidence for correlation with asymptomatic trees [86] or if new genotypes have been trends in changing conditions such as changes in tempera- introduced to a region [87], well-planed hierarchical sam- ture (at different seasons) and precipitation (e. g. amount, pling can also determine if there is structure within popula- time and frequency of occurrence, type, persistence). Both tions [88]. Numerous population genetics studies have been long- and short-term changes can result in a disease out- undertaken considering invasive pathogens [15], but there break. Short-term weather data can be obtained in diverse are few examples with native pathogens. manners (weather stations, on-site temperature/humidity The presence of the pathogen across the range of the host recording devices such as iButtons) and combined with data and its isolation from asymptomatic trees provide strong evi- (e.g. plant composition, growth rate, tree health, ground dence for it being native rather than alien; this is an impor- cover, litter depth) from long-term monitoring plots. Any tant distinction as if it is an introduced alien pathogen, changes in weather at either a local or landscape scale could appropriate management goals should be determined, e.g. then be related to changes found in the type and amount assessment of eradication feasibility, development of con- of damage present. Plant-based indicators are an alterna- tainment and disease mitigation strategies [7, 89]. For native tive way to explore the change in climatic conditions and/ pathogens, the expectation is that they will have a ubiquitous or effect of such changes. These include, for example, stud- distribution, and management must focus on the release of ies of tree rings (which can link tree declines to changes in the stressors driving the pathogen emergence. atmospheric conditions) or taking leaf samples and using C isotopic signature (δ13C) to obtain information regarding Step 3. Is the disease associated with land-use change water scarcity. or human disturbance? Step 5. Have there been changes in other abiotic fac- For this purpose, landscape-level studies of disease tors? extent and distribution are required. Variables at this level include those related to human disturbance, e.g. distance to There are numerous additional abiotic factors, many of roads and hiking trails, changes in forest management (e.g. which may be linked to the anthropogenic changes observed changes in logging regimes), and air and water pollution in step 3, which may contribute to the incidence and severity and other plot variables (e.g. average age of individuals per of a disease outbreak. These include changes to soil structure 1 3 120 Current Forestry Reports (2022) 8:111–123 due to compaction or other factors, changes in fire regimes, ecosystem’ approach incorporates both biotic and abiotic increased nutrients or imbalanced nutrients due to fertiliser aspects of a forest community and the multiple interactions use, pesticide and herbicide damage, changes in soil pH, amongst host, pathogen, mutualists, the environment and increased salinity or altered drainage or water tables due to humans. A ‘whole ecosystem’ approach highlights the many land-use management. These geophysical and hydrophysical aspects and entanglements of forest declines and enables us changes will predominantly affect the host physiology and to respond with management options appropriate to each may reduce the hosts’ disease resistance. scenario. The framework proposed here provides a logical six-step approach to discovering the direct and indirect envi- Step 6. Have there been changes in other biotic fac- ronmental drivers of a forest decline syndrome. tors? Funding Open Access funding enabled and organized by CAUL and As with step 5, numerous potential biotic interactions its Member Institutions JO was supported by the ‘Ramón y Cajal’ fel- may influence a disease outbreak, and again many of these lowship RYC-2015–17459 from the Ministry of Science and Educa- will be linked to anthropogenic disturbance: changes in veg- tion of Spain. USDA Forest Service Forest Health Protection partially etation (stand structure, abundance, composition, density, supported MLS. basal area age) due to edge effects, invasion by alien plant species, other pests and diseases, rhizosphere biota changes Declarations and mycorrhiza. These other biotic impacts could also be the Conflict of Interest The authors declare no competing interests. result of climate, weather, land use, human disturbance and management and belowground changes and would indicate Human and Animal Rights and Informed Consent This article does not a complex interactive scenario, for example, rhizosphere- contain any studies with human or animal subjects performed by any of the authors. plant-pathogen interactions. Changes in belowground microbial composition can result from changes in soil condition and plant communities, Open Access This article is licensed under a Creative Commons Attri- which, in turn, can be affected by human disturbances and bution 4.0 International License, which permits use, sharing, adapta- tion, distribution and reproduction in any medium or format, as long changes in management. The most complex and challenging as you give appropriate credit to the original author(s) and the source, aspect of understanding tree declines with complex aetiolo- provide a link to the Creative Commons licence, and indicate if changes gies is attempting to unravel these relationships. were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not Conclusion permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a Due to global change, more trees will exhibit a wide range of copy of this licence, visit http://cr eativ ecommons. or g/licen ses/ b y/4.0/ . symptoms indicative of poor vigour, particularly in stressed species towards the limit of their native ranges and stands growing on marginal sites. By looking at four paradigmatic examples of forest decline, we found forest management had References a significant role as predisposing and inciting factors for tree health. Land-use change is one of the three components Papers of particular interest, published recently, have been highlighted as: of global change, including both climate change and glo- balisation, and more attention should be placed on its role • Of importance •• Of major importance on tree health. The prevalence of diseases caused by native pathogens with complicated aetiologies will increase, and 1. Ramsfield TD, Bentz BJ, Faccoli M, Jactel H, Brockerhoff EG. interdisciplinary teams are needed to untangle the multiple Forest health in a changing world: effects of globalization and biotic and abiotic causative factors and their interactions climate change on forest insect and pathogen impacts. Forestry. to reveal the primary drivers of the decline. Recognition, 2016;89:245–52. 2. Agrios GN. Plant Pathology. Fifth ed. Elsevier Academic Press, characterisation and management of these epidemics are challenging as native pathogens are often already wide- 3. Burgess TI, Wingfield MJ. Impact of fungi in natural forest eco- spread, and eradication is not viable. The next century will systems; a focus on Eucalyptus. In: Sivasithamparam K, Dixon likely see an unprecedented rise in forest pathogen epidem- KW, Barrett RL, editors. Microorganisms in plant conservation and biodiversity. Dordrecht: Kluwer Academic Publishers; 2002. ics, both native and alien; there is a need for a predictive p. 285–306. rather than a reactive response. Rather than focusing on ‘single pathogen-single host’ disease dynamics, a ‘whole 1 3 Current Forestry Reports (2022) 8:111–123 121 4. Burdon JJ, Thrall PH. Coevolution of plants and their pathogens 24. Paap T, Burgess TI, McComb JA, Shearer BL, Hardy GES. in natural habitats. Science. 2009;324:755–6. Quambalaria species, including Q. coyrecup sp. nov., impli- 5. Stenlid J, Oliva J. Phenotypic interactions between tree hosts and cated in canker and shoot blight diseases causing decline of invasive forest pathogens in the light of globalization and climate Corymbia species in the southwest of Western Australia. change. Philos Trans R Soc B Biol Sci. 2016;371:20150455. Mycol Res. 2008;112:57–69. 6. Anderson PK, Cunningham AA, Patel NG, Morales FJ, Epstein 25. Paap T, Burgess TI, Calver M, McComb J, Shearer B, Hardy PR, Daszak P. Emerging infectious diseases of plants: pathogen GES. A thirteen-year study on the progression of a severe can- pollution, climate change and agrotechnology drivers. Trends ker disease on the health of a keystone tree in a Mediterranean Ecol Evol. 2004;19:535–44. forest and woodland ecosystem. For Pathol. 2017;47:e12292. 7. Paap T, Wingfield MJ, Burgess TI, Wilson JRU, Richardson DM, 26. Ramalho CE, Laliberté E, Poot P, Hobbs RJ. Complex effects Santini A. Invasion frameworks: a forest pathogen perspective. of fragmentation on remnant woodland plant communi- Curr For Rep. 2022; 8:74–89 ties of a rapidly urbanizing biodiversity hotspot. Ecology. 8. Bonnamour A, Gippet JMW, Bertelsmeier C. Insect and plant 2014;95:2466–78. invasions follow two waves of globalisation. Ecol Lett. 2021. 27. Zambrano J, Garzon-Lopez CX, Yeager L, Fortunel C, Cordeiro https:// doi. org/ 10. 1111/ ele. 13863. NJ, Beckman NG. The effects of habitat loss and fragmentation 9. Rizzo DM, Garbelotto M. Sudden oak death: endangering on plant functional traits and functional diversity: what do we California and Oregon forest ecosystems. Front Ecol Environ. know so far? Oecologia. 2019;191:505–18. 2003;1:197–204. 28. Arroyo-Rodríguez V, Saldana-Vazquez RA, Fahrig L, Santos 10. Rigling D, Prospero S. Cryphonectria parasitica, the causal BA. Does forest fragmentation cause an increase in forest tem- agent of chestnut blight: invasion history, population biology perature? Ecol Res. 2017;32:81–8. and disease control. Mol Plant Pathol. 2018;19:7–20. 29. Latimer CE, Zuckerberg B. Forest fragmentation alters winter 11. Shearer BL, Crane CE, Barrett S, Cochrane A. Phytophthora cin- microclimates and microrefugia in human-modified landscapes. namomi invasion, a major threatening process to conservation of Ecography. 2017;40:158–70. flora diversity in the South-west Botanical Province of Western 30. Watson JEM, Evans T, Venter O, Williams B, Tulloch A, Stewart Australia. Aust J Bot. 2007;55:225–38. C, et al. The exceptional value of intact forest ecosystems. Nat 12. Brasier CM, Buck KW. Rapid evolutionary changes in a globally Ecol Evol. 2018;2:599–610. invading fungal pathogen (Dutch elm disease). Biol Invasions. 31.•• Paap T, Burgess TI, Rolo V, Steel E, Hardy GESJ. Anthropo- 2001;3:223–33. genic disturbance impacts stand structure and susceptibility 13. Pautasso M, Aas G, Queloz V, Holdenrieder O. European ash of an iconic tree species to an endemic canker pathogen. For (Fraxinus excelsior) dieback–a conservation biology challenge. Ecol Manag. 2018;425:145–53. Data driven paper based on Biol Cons. 2013;158:37–49. extensive surveys showing a clear evidence for anthropogenic 14.•• Desprez-Loustau M-L, Aguayo J, Dutech C, Hayden KJ, Hus- disturbance driving a tree decline. son C, Jakushkin B, et al. An evolutionary ecology perspective 32. Dawes W, Ali R, Varma S, Emelyanova I, Hodgson GA, McFar- to address forest pathology challenges of today and tomorrow. lane DJ. Modelling the effects of climate and land cover change Ann For Sci. 2016;73:45–67. An important review highlight- on groundwater recharge in southwest Western Australia. Hydrol ing the need to consider evolutionary ecology perspectives Earth Syst Sci. 2012;16:2709–22. in forest health research. The authors also provide policy 33. Matusick G, Ruthrof KX, Kala J, Brouwers NC, Breshears DD, recommendations and identify areas of research need. Hardy GES. Chronic historical drought legacy exacerbates 15. Burgess TI, Wingfield MJ. Pathogens on the move: a 100 tree mortality and crown dieback during acute heatwave-com- year global experiment with planted eucalypts. Bioscience. pounded drought. Environ Res Lett. 2018;13:095002. 2017;67:14–25. 34. Ruthrof KX, Breshears DD, Fontaine JB, Froend RH, Matusick 16.•• Ghelardini L, Pepori AL, Luchi N, Capretti P, Santini A. Driv- G, Kala J, et al. Subcontinental heat wave triggers terrestrial and ers of emerging fungal diseases of forest trees. For Ecol Manag. marine, multi-taxa responses. Sci Rep. 2018;8:1–9. 2016;381:235–46. Provides an overview of host-pathogen- 35.• Sapsford SJ, Paap T, Hardy GESJ, Burgess TI. Anthropogenic environment relationships with emphasis on interactions disturbance impacts mycorrhizal communities and abiotic soil among anthropogenic disturbance, new and emerging fungi properties: implications for an endemic forest disease. Front For (i.e. invasive species, new strains, new hybrids and latent Glob Chang. 2021;3:e593243. Strong empirical evidence for pathogens) and potential range shifts of fungi. the complex interactions between tree decline and soil biota. 17. Hepting GH. Climate and forest diseases. Annu Rev Phytopathol. 36. Guo Q, Riitters KH, Potter KM. A subcontinental analysis of for- 1963;1:31–50. est fragmentation effects on insect and disease invasion. Forests. 18. Hennon PE, Frankel SJ, Woods AJ, Worrall JJ, Norlander D, 2018;9:744. Zambino PJ, et al. A framework to evaluate climate effects on 37. Burgess TI, Scott JK, McDougall KL, Stukely MJC, Crane C, forest tree diseases. For Pathol. 2020;50:e12649. Dunstan WA, et al. Current and projected global distribution of 19. Sinclair WA. Comparisons of recent declines of white ash, Phytophthora cinnamomi, one of the world’s worst plant patho- oaks, and sugar maple in northeastern woodlands. Cornell gens. Glob Change Biol. 2017;23:1661–74. Plantations. 1965;20:62–7. 38. Paap T, Brouwers N, Burgess TI, Hardy GES. Importance of 20. Manion PD. Tree disease concepts. New Jersey: Prentice-Hall; climate, anthropogenic disturbance and pathogens (Quamba- 1981. laria coyrecup and Phytophthora spp.) on marri (Corymbia 21. Manion PD. Tree disease concepts. Englewood Cliffs: Prentice calophylla) tree health in southwest Western Australia. Ann For Hall; 1991. Sci. 2017;74:62. 22. Holdenrieder O, Pautasso M, Weiberg PJ, Lonsdale D. Tree 39. Croeser L, Admiraal R, Barber PA, Burgess TI, Hardy GESJ. diseases and landscape processes: the challenge of landscape Reflectance spectroscopy to characterise the response of Corym - pathology. Trends Ecol Evol. 2004;19:446–52. bia calophylla to Phytophthora root rot and waterlogging stress. 23. Desprez-Loustau M-L, Marçais B, Nageleisen LM, Piou D, Forestry. 2021. https:// doi. org/ 10. 1093/ fores try/ cpab0 45. 40. Corcobado T, Vivas M, Moreno G, Solla A. Ectomycorrhizal Vannini A. Interactive effects of drought and pathogens in symbiosis in declining and non-declining Quercus ilex trees forest trees. Ann For Sci. 2006;63:597–612. 1 3 122 Current Forestry Reports (2022) 8:111–123 infected with or free of Phytophthora cinnamomi. For Ecol Man- New England and linking disease incidence with tree size, age. 2014;324:72–80. stand density and soil type. 41. Ennos RA. Resilience of forests to pathogens: an evolutionary 59.•• Schulz AN, Mech AM, Asaro C, Coyle DR, Cram MM, ecology perspective. Forestry. 2015;88:41–52. Lucardi RD, et al. Assessment of abiotic and biotic factors 42. Hossain M, Veneklaas EJ, Hardy GESJ, Poot P. Tree host–patho- associated with eastern white pine (Pinus strobus L.) dieback gen interactions as influenced by drought timing: linking physi- in the Southern Appalachian Mountains. For Ecol Manag. ological performance, biochemical defence and disease severity. 2018;423:59–69. This paper considers numerous biotic and Tree Physiol. 2019;39:6–18. abiotic factors driving the landscape level impacts of white 43. Camarero JJ, Bigler C, Linares JC, Gil-Pelegrín E. Synergistic pine dieback. effects of past historical logging and drought on the decline of 60. Livingston WH, Kenefic LS. Low densities in white pine Pyrenean silver fir forests. For Ecol Manage. 2011;262:759–69. stands reduce risk of drought-incited decline. For Ecol Manage. 44. Oliva J, Colinas C. Canopy openings may prevent fir broom rust 2018;423:84–93. (Melampsorella caryophyllacearum) infections. Eur J For Res. 61. Costanza KKL, Whitney TD, McIntire CD, Livingston WH, 2007;126:507–11. Gandhi KJK. A synthesis of emerging health issues of eastern 45.•• Oliva J, Colinas C. Decline of silver fir (Abies alba Mill.) stands white pine (Pinus strobus) in eastern North America. For Ecol in the Spanish Pyrenees: role of management, historic dynamics Manage. 2018;423:3–17. and pathogens. For Ecol Manag. 2007;252:84–97. Good exam- 62. Costanza KKL, Crandall MS, Rice RW, Livingston WH, Munck ple of how to try to understand forest decline at a large scale IA, Lombard K. Economic implications of a native tree dis- by sampling stands at random and trying to link poor health ease, Caliciopsis canker, on the white pine (Pinus strobus) lum- with different pathogens. ber industry in the northeastern United States. Can J For Res. 46. Johannesson H, Stenlid J. Molecular identification of wood- 2019;49:521–30. inhabiting fungi in an unmanaged Picea abies forest in Sweden. 63. Hayhoe K, Wake CP, Huntington TG, Luo L, Schwartz For Ecol Manage. 1999;115:203–11. MD, Sheffield J, et  al. Past and future changes in climate 47. Oliva J, Colinas C. Epidemiology of Heterobasidion abietinum and hydrological indicators in the US Northeast. Clim Dyn. and Viscum album on silver fir (Abies alba) stands of the Pyr - 2007;28:381–407. enees. For Pathol. 2010;40:19–32. 64. Hayhoe K, VanDorn J, Croley T II, Schlegal N, Wuebbles D. 48. Oliva J, Suz LM, Colinas C. Ecology of Armillaria species on Regional climate change projections for Chicago and the US silver fir (Abies alba) in the Spanish Pyrenees. Ann For Sci. Great Lakes. J Great Lakes Res. 2010;36:7–21. 2009;66:603. 65.•• Simler-Williamson AB, Rizzo DM, Cobb RC. Interacting effects 49.•• Sangüesa-Barreda G, Camarero JJ, Oliva J, Montes F, Gazol of global change on forest pest and pathogen dynamics. Ann Rev A. Past logging, drought and pathogens interact and contribute Ecol Evol Syst. 2019;50:381–403. Review paper summariz- to forest dieback. Agric For Meteorol. 2015;208:85–94. Shows ing the interactions between tree mortality, pathogens, pests, how declining trees were mostly dominant or co-dominant the environment and climate change. The authors develop trees that were released after selective cuttings. a framework to explain how diverse global change drivers 50. Améztegui A, Brotons L, Coll L. Land-use changes as major impact the disease triangle. drivers of mountain pine (Pinus uncinata Ram) expansion in the 66. Wyka SA, Smith C, Munck IA, Rock BN, Ziniti BL, Broders Pyrenees. Glob Ecol Biogeogr. 2010;19:632–41. K. Emergence of white pine needle damage in the north- 51. Slippers B, Hurley BP, Wingfield MJ. Sirex woodwasp: a model eastern United States is associated with changes in pathogen for evolving management paradigms of invasive forest pests. pressure in response to climate change. Glob Change Biol. Annu Rev Entomol. 2015;60:601–19. 2017;23:394–405. 52. Camarero JJ, Gazol A, Sangüesa-Barreda G, Oliva J, Vicente- 67. Munck IA, Luther T, Wyka S, Keirstead D, McCracken K, Serrano SM. To die or not to die: early warnings of tree dieback Ostrofsky WD, et al. Soil and stocking effects on Caliciopsis in response to a severe drought. J Ecol. 2015;103:44–57. canker of Pinus strobus L. Forests. 2016;7:269. 53. Macias M, Andreu L, Bosch O, Camarero JJ, Gutiérrez E. 68.• Costanza KKL, Livingston WH, Fraver S, Munck IA. Dendro- Increasing aridity is enhancing silver fir (Abies alba mill.) chronological analyses and whole-tree dissections reveal Cali- water stress in its south-western distribution limit. Clim Chang. ciopsis canker (Caliciopsis pinea) damage associated with the 2006;79:289–313. declining growth and climatic stressors of eastern White Pine 54. Gazol A, Camarero JJ, Gutiérrez E, Popa I, Andreu-Hayles L, (Pinus strobus). Forests. 2020;11:347. Paper that used den- Motta R, et al. Distinct effects of climate warming on popu - drochronology and whole-tree dissection to link a decrease in lations of silver fir (Abies alba) across Europe. J Biogeogr. tree growth to tree damage, i.e. cankers with abiotic stressors 2015;42:1150–62. (weather events—droughts and a hurricane). 55. Marqués L, Peltier DMP, Camarero JJ, MlA Zavala, Madrigal- 69. Whitney TD, Cram MM, Barnes BF, Yao J, Lucardi RD, Gandhi González J, Sangüesa-Barreda G, et al. Disentangling the lega- KJK. Tree-level distribution of a novel insect-pathogen complex cies of climate and management on tree growth. Ecosystems. and its potential contribution to eastern white pine dieback. For 2021. https:// doi. org/ 10. 1007/ s10021- 021- 00650-8. Ecol Manage. 2018;423:49–58. 56. Peck C. Annual report on the New York State Museum of 70. Mech AM, Asaro C, Cram MM, Coyle DR, Gullan PJ, Cook Natural History. Report of the botanist. Albany, Regents of LG, et al. Matsucoccus macrocicatrices (Hemiptera: Matsucoc- the University of the State of New York. 1980. Available at: cidae): first report, distribution, and association with sympto- https:// www. biodi versi tylib rary. org/ item/ 110212. matic eastern white pine in the southeastern United States. J 57. Fitzpatrick HM. Monograph of the Coryneliaceae. Mycologia. Econ Entomol. 2013;106:2391–8. 1920;12:206–37. 71. Broders K, Munck I, Wyka S, Iriarte G, Beaudoin E. Charac- 58.•• Munck IA, Livingston WH, Lombard K, Luther T, Ostrofsky terization of fungal pathogens associated with white pine nee- WD, Weimer J, et al. Extent and severity of Caliciopsis canker dle damage (WPND) in northeastern North America. Forests. in New England, USA: an emerging disease of eastern white 2015;6:4088–104. pine (Pinus strobus L.). Forests. 2015;6:4360–73. One of the 72. Livingston WH, Munck I, Lombard K, Weimer J, Bergdahl first papers describing the extent of Caliciopsis canker in A, Kenefic LS et  al. MP764: Field Manual for Managing 1 3 Current Forestry Reports (2022) 8:111–123 123 Eastern White Pine Health in New England. Maine Agricul- endangered monkey puzzle tree (Araucaria araucana) in Chile. tural and Forest Experiment Station Miscellaneous Publications. Biol Cons. 2012;152:110–8. 2019. https://digit alc ommons. libr ar y.umaine. edu/ aes_ miscp ubs/ 82. Shepherd JD, Ditgen RS. Human use and small mammal com- 24 munities of Araucaria forests in Neuquén, Argentina. Mastozo- 73. Vélez ML, Marfetán JA, Salgado Salomon ME, Taccari LE. ología Neotropical. 2005;12:217–26. Mortierella species from declining Araucaria araucana trees in 83. Cóbar-Carranza AJ, García RA, Pauchard A, Pena E. Effect of Patagonia Argentina. For Pathol. 2020;50:e12591. Pinus contorta invasion on forest fuel properties and its poten- 74. Balocchi F, Wingfield MJ, Ahumada R, Barnes I. Pewenomy - tial implications on the fire regime of Araucaria araucana and ces kutranfy gen. nov. et sp. nov. causal agent of an important Nothofagus antarctica forests. Biol Invasions. 2014;16:2273–91. canker disease on Araucaria araucana in Chile. Plant Pathol. 84. Molina JR, Martin A, Drake F, Martín LM, Herrera MÁ. Frag- 2021;70:1243–59. mentation of Araucaria araucana forests in Chile: quantification 75. Vélez ML, Salgado Salomón ME, Marfetan A, Tirante SI, Mattes and correlation with structural variables. iForest-Biogeosci For. Fernández H, Avila M, Caracterización desecación del dosel y 2015;9:244. sanidad de Araucaria araucana en Argentina. Technical Report. 85. Dash JP, Watt MS, Pearse GD, Heaphy M, Dungey HS. Assess- 2018. Available from: https:// doi. org/ 10. 13140/ RG.2. 2. 14227. ing very high resolution UAV imagery for monitoring forest 78889. health during a simulated disease outbreak. ISPRS J Photo- 76. Garreaud RD, Boisier JP, Rondanelli R, Montecinos A, gramm Remote Sens. 2017;131:1–14. Sepúlveda HH, Veloso-Aguila D. The central Chile mega 86. Dakin N, White D, Hardy GES, Burgess TI. The opportunis- drought (2010–2018): a climate dynamics perspective. Int J tic pathogen, Neofusicoccum australe, is responsible for crown Climatol. 2020;40:421–39. dieback of peppermint (Agonis flexuosa) in Western Australia. 77. Cordero RR, Asencio V, Feron S, Damiani A, Llanillo PJ, Australas Plant Pathol. 2010;39:202–6. Sepulveda E, et al. Dry-season snow cover losses in the Andes 87. Dutech C, Barrès B, Bridier J, Robin C, Milgroom MG, Ravigné (18°–40° S) driven by changes in large-scale climate modes. Sci V. The chestnut blight fungus world tour: successive introduction Rep. 2019;9:1–10. events from diverse origins in an invasive plant fungal pathogen. 78.• Moreno-Gonzalez R, Giesecke T, Fontana SL. The impact of Mol Ecol. 2012;21:3931–46. recent land-use change in the Araucaria araucana forest in 88. McDonald BA, Linde C. Pathogen population genetics, evolu- northern Patagonia. Holocene. 2020;30:1101–14. Holistic study tionary potential and durable resistance. Annu Rev Phytopathol. of different types of impacts and how they effect a forest. 2002;40:349–79. 79. Mundo IA, Kitzberger T, Juñent FAR, Villalba R, Bar- 89. Paap T, Wingfield MJ, Burgess TI, Hulbert JM, Santini A. Har - rera MD. Fire history in the Araucaria araucana forests of monising the fields of invasion science and forest pathology. Argentina: human and climate influences. Int J Wildland Fire. NeoBiota. 2020;62:301–32. 2012;22:194–206. 80. Aagesen DL. Indigenous resource rights and conservation of Publisher's Note Springer Nature remains neutral with regard to the monkey-puzzle tree (Araucaria araucana, Araucariaceae): jurisdictional claims in published maps and institutional affiliations. a case study from southern Chile. Econ Bot. 1998;52:146–60. 81. Zamorano-Elgueta C, Cayuela L, González-Espinosa M, Lara A, Parra-Vázquez MR. Impacts of cattle on the South Ameri- can temperate forests: challenges for the conservation of the 1 3

Journal

Current Forestry Reports – Springer Journals

Published: Jun 1, 2022

Keywords: Abies alba; Araucaria araucana; Corymbia calophylla; Global change; Pinus strobus; Tree decline

There are no references for this article.