FEATUREOpen Access icon OPENOpen Access license

Endemic and Emerging Pathogens Threatening Cork Oak Trees: Management Options for Conserving a Unique Forest Ecosystem

    Authors and Affiliations
    • Salvatore Moricca , Dipartimento di Scienze delle Produzioni Agroalimentari e dell’Ambiente (DISPAA), Sezione di Patologia Vegetale ed Entomologia, Università degli Studi di Firenze, 50144 Firenze, Italy
    • Benedetto T. Linaldeddu , Dipartimento di Agraria, Sezione di Patologia Vegetale ed Entomologia, Università degli Studi di Sassari, 07100, Sassari, Italy
    • Beatrice Ginetti , Dipartimento di Scienze delle Produzioni Agroalimentari e dell’Ambiente (DISPAA), Sezione di Patologia Vegetale ed Entomologia, Università degli Studi di Firenze, 50144 Firenze, Italy
    • Bruno Scanu , Dipartimento di Agraria, Sezione di Patologia Vegetale ed Entomologia, Università degli Studi di Sassari, 07100, Sassari, Italy
    • Antonio Franceschini , Dipartimento di Agraria, Sezione di Patologia Vegetale ed Entomologia, Università degli Studi di Sassari, 07100, Sassari, Italy
    • Alessandro Ragazzi , Dipartimento di Scienze delle Produzioni Agroalimentari e dell’Ambiente (DISPAA), Sezione di Patologia Vegetale ed Entomologia, Università degli Studi di Firenze, 50144 Firenze, Italy

      Published Online:https://doi.org/10.1094/PDIS-03-16-0408-FE


      Cork oak (Quercus suber) forests are economically and culturally intertwined with the inhabitants of the Mediterranean basin and characterize its rural landscape. These forests cover over two million hectares in the western Mediterranean basin and sustain a rich biodiversity of endemisms as well as representing an important source of income derived from cork production. Currently cork oak forests are threatened by several factors including human-mediated disturbances such as poor or inappropriate management practices, adverse environmental conditions (irregular water regime with prolonged drought periods), and attacks of pathogens and pests. All these adverse factors can interact, causing a complex disease commonly known as “oak decline.” Despite the numerous investigations carried out so far, decline continues to be the main pathological problem of cork oak forests because of its complex etiology and the resulting difficulties in defining suitable control strategies. An overview of the literature indicates that several pathogenic fungi and oomycota can play a primary role in the etiology of this syndrome. Therefore, the aim of this review is to analyze the recent advances achieved regarding the bio-ecology of the endemic and emerging pathogens that threaten cork oak trees with particular emphasis on the species more directly involved in oak decline. Moreover, the effect of climate change on the host-pathogen interactions, a task fundamental for making useful decisions and managing cork oak forests properly, is considered.

      Cork oak (Quercus suber) is an evergreen oak tree native to southwest Europe and northwest Africa. The few relict areas of southeast Italy constitute the far eastern limit of the species (Beccarisi et al. 2010). Cork oak ecosystems include a mosaic of habitats spanning from open savanna-like formations to closed sclerophyll forests as a result of the long-term human presence and related activities in this area (Blondel 2006; Bugalho et al. 2011). These heterogeneous forest ecosystems cover over two million hectares in the western Mediterranean basin where they sustain a rich biodiversity of endemisms as well as representing an important source of income derived from cork production (Campos et al. 2008; Marañón et al. 1999).

      Cork production is an additional source of income to farmers, supplementing that generated by traditional agricultural, silvicultural, and pastoral activities (Pinto-Correia 2000). Cork processing is a thriving industry that involves a number of small and medium sized enterprises and provides employment in less developed areas of southern Europe (Goncalves 2000). However, the progressive reduction in the market price of cork is contributing to a progressive abandonment of cork oak forests and subsequent shrub encroachment in several areas in southwestern Europe (Pinto-Correia 1993). Without proper management, these fragile ecosystems are quickly overgrown by Mediterranean matorral species, such as Cistus species, which in turn promote an increased risk of wildfires and loss of habitats and biodiversity (Acácio et al. 2009).

      In contrast, high anthropogenic pressure, consisting of overgrazing and irregular cutting of firewood, is contributing to the degradation of cork oak ecosystems in some areas (Campos et al. 2007). Overall, the abandonment of traditional land management activities, associated with land use transformations, have led to a progressive loss in cork oak forests (Costa et al. 2011). In addition, during the last decades, tree mortality events have occurred with an increasing frequency in several cork oak forests in the Mediterranean basin, contributing to a further degradation of these woodlands (Brasier 1992; Costa et al. 2010; Franceschini et al. 1999).

      Cork oak suffers from few major disease problems. In literature, more than 300 species of fungi and oomycota are reported on cork oak, of which at least 100 are pathogenic (Franceschini et al. 1993; Luque et al. 2000). Fortunately, very few are primary pathogens able to attack healthy tree tissues, the majority being opportunistic pathogens that colonize oak tissues when they have been previously weakened by abiotic or biotic factors (Luque et al. 2000). Recently, some species of opportunistic fungi have received greater attention, because they can colonize oak tissues as endophytes without inducing disease symptoms for a long time (Gonthier et al. 2006; Moricca et al. 2012). Healthy, unstressed trees normally manage to keep these endophytes under control, so that the trees do not suffer or exhibit symptoms, even though they are colonized (balanced antagonism) (Ragazzi and Moricca 2012; Schulz and Boyle 2005). However, when the trees become weakened by environmental stress factors, these fungi, initially confined, can colonize adjacent tissues, causing a progressive decline and eventually the death of the tree (Moricca and Ragazzi 2008; Saikkonen et al. 1998). There is some evidence to suggest that regional increases in the frequency and severity of droughts, combined with higher temperatures, are specifically selective for those cork oak pathogens that are most thermotolerant, and that some of these pathogens, combined with climate-driven physiological stress, then cause increasing decline and higher mortality rates in cork oaks (Desprez-Loustau et al. 2006; Picco et al. 2011).

      Oak decline is commonly considered a multifactorial disease in which many interacting abiotic and biotic factors such as drought, frost, insect pests, and pathogens, variable in type, intensity, and frequency even at site level are involved (Inácio et al. 2011; Linaldeddu et al. 2011; Moreira and Martins 2005; Ragazzi et al. 1995). The effects of these factors have long been synthesized in a theoretical model that hypothesizes the succession of three different types of factors predisposing, inciting, and contributing (Manion 1991). It has, however, been shown that pathogens belonging to the genera Diplodia and Phytophthora have had a prominent role in the decline and mortality of oak trees in a variety of contexts (Linaldeddu et al. 2014; Lynch et al. 2013; Perez-Sierra et al. 2013; Scanu et al. 2013).

      The aim of this review is to analyze the recent advances achieved regarding the bio-ecology of the endemic and emerging pathogens that threaten cork oak trees with particular emphasis on the species more directly involved in the etiology of oak decline. Pathogens are dealt with according to the tree portions in which they mainly occur: the leaves, stems, and roots. The means to control the most deleterious agents are also discussed, with an emphasis on environmentally friendly control measures. Gaps in our knowledge of cork oak pathogens, their reproductive strategy, and dispersal ability within the cork oak range are outlined.

      Leaf Pathogens

      The most commonly observed leaf spot causing-agents of cork trees include Discula quercina (Fig. 1A), Cystodendron dryophilum (Fig. 1B), Lembosia quercina (Fig. 1C), and Dendrophoma myriadea (Fig. 1D). It is well known that leaf diseases can weaken trees by interrupting photosynthesis, respiration rate, and the metabolic pathways, and by impairing thermal regulation (Marçais and Desprez-Loustau 2014). However, to date, little information is available about pathogenicity, geographic distribution, oak host range, and genetic variability in any country of the main cork oak leaf pathogens. Another major gap in knowledge about cork oak-leaf pathogen interactions in natural ecosystems concerns the proximal mechanisms of leaf infection. In addition, for all these species except D. quercina, there are no nucleotide sequences available in public databases, and no ex-type cultures are known to exist.

      Fig. 1.

      Fig. 1. Foliar diseases caused by some cork oak pathogens. A, leaf necroses induced by the anthracnose agent Discula quercina, with black acervuli that are prominent on the upper surface of the lesions. B, leathery-brown, necrotic leaf spots with a distinct, dark-line margin caused by Cystodendron dryophilum. C, small, scattered, black-to-velvety leaf spots with a regular margin caused by Lembosia quercina. D, leaf tip and marginal necroses, with distinct, reddish-brown edges produced by Dendrophoma myriadea.

      Download as PowerPoint

      The ascomycete D. quercina (Fig. 1A), known to cause anthracnose, shoot blight, and twig cankers on oaks in North America and Europe, is probably the species most studied (Hecht-Poinar and Parmeter 1986; Moricca and Ragazzi 2008, 2011; Ragazzi et al. 2002, 2007b). On cork oak, D. quercina causes dark brown-to-black leaf spots, coalescing into larger necrotic areas at the end of the growing season; sometimes it also causes twig cankers. At the physiological level, infection of D. quercina on cork oak modifies the normal balance of some metabolic processes, including stomatal conductance and photosynthesis (Linaldeddu et al. 2009b). D. quercina has been shown to produce in vitro several secondary bioactive metabolites, some of which are phytotoxic (Maddau et al. 2011). In autumn, this pathogen produces on leaves several black and erumpent acervular conidiomata, which are the main source of inoculum (Marras 1962a). The sexual phase (Apiognomonia quercina) develops very rarely on cork oak. In contrast, on deciduous oaks, the differentiation of perithecia is more common; in turkey oak, for instance, D. quercina usually overwinters as ascomata on fallen leaves, and during the growing season the sexual spores produce primary infections on the buds, shoots, and expanding leaves (Ragazzi et al. 1999). D. quercina also survives as an endophyte in the asymptomatic tissues of healthy and declining oak trees (Linaldeddu et al. 2011).

      C. dryophilum causes characteristic, leathery-brown zonate spots with a distinct margin (Fig. 1B), whereas L. quercina causes typical, scab-like, dark and velvety spots (Fig. 1C). Attacks of both these fungi are reported in dense stands with an abundant overstory, where they cause a slow but gradual and sometimes total defoliation (Marras 1962a). Both pathogens differentiate their asexual reproductive structures in springtime (May-June): C. dryophilum on the lower leaf blade and L. quercina on the upper leaf blade, mainly in the center of spots. Most knowledge on the biology of C. dryophilum and L. quercina comes from Sardinia (Italy), and relatively little is known about these species in other Mediterranean countries.

      D. myriadea causes a leaf-tip necrosis (Fig. 1D), mainly in autumn, when light-brown necrotic areas appear at the leaf tip; these areas have a distinct reddish-brown edge that distinguishes them clearly from the still healthy dark-green leaf. Symptomatic leaves look scorched and are easily recognized from afar. The fungus is fairly rare, but on the trees its infection may be severe. Pathogenicity tests on seedlings have confirmed the virulence of this pathogen (Luque et al. 2000).

      Other leaf pathogens on cork oaks are Erysiphe spp. (previously reported as Microsphaera alphitoides), which causes powdery mildew, and the oak rust agent Uredo quercus (Marras 1962a). To date, there is little information on the ecological impact and role played by these leaf pathogens in the etiology of cork oak decline. All of these leaf pathogens are endemic to the Mediterranean region and do not require preventive or curative measures. Some are controlled by natural competitors. For example, the oak rust pathogen U. quercus is commonly controlled in nature by Sphaerellopsis filum, a nonspecific rust hyperparasite (Ragazzi et al. 2007a).

      Stem, Branch, and Twig Pathogens

      Several ascomycete fungi are reported in literature as agents of cankers and dieback of cork oak trees. These pathogens cause local infections on trunk, branches, and twigs, variable in severity and incidence. Since the early 1980s, some of these fungi have received increasing attention because they have consistently been associated with etiology of cork oak mortality in many countries (Franceschini et al. 1999; Luque and Girbal 1989).

      Two species in particular, Diplodia corticola and Biscogniauxia mediterranea, were found to be the most widely distributed pathogens in declining cork oak forests; the first has been considered the most virulent cork oak pathogen (Linaldeddu et al. 2009b; Luque et al. 2000). Attacks of D. corticola, originally misidentified as Diplodia mutila, were reported on cork oak trees in Italy, Morocco, Portugal, Spain, and Tunisia (Alves et al. 2004). The pathogen also affects other Mediterranean oak species such as Quercus afares, Q. canariensis, Q. coccifera, and Q. ilex (Linaldeddu et al. 2009a, 2014; Tsopelas et al. 2010). In recent years, D. corticola has caused concern in the United States, where it colonized aggressively Q. agrifolia, Q. rubra, and Q. virginiana (Aćimović et al. 2016; Dreaden et al. 2011; Lynch et al. 2013). Despite the number of studies aimed at elucidating the taxonomy and pathogenicity of D. corticola, its evolutionary and geographical origins remain unresolved. Phylogenetic analyses based on ITS and tef1-α sequences of isolates from different countries revealed the existence of two distinct evolutionary lineages with a different geographic distribution (Linaldeddu et al. 2013). More recently, another canker-causing agent, described as Diplodia quercivora, phylogenetically very closely related to D. corticola, was reported on declining Q. canariensis trees in Tunisia (Linaldeddu et al. 2013) and on Q. virginiana in Florida (Dreaden et al. 2014a). These two taxa were accommodated in the subclade 4, a distinct group within Diplodia genus, which includes only species known primarily as oak pathogens (Alves et al. 2014). The two species can be distinguished from each other and from other Diplodia species by morphology and DNA sequence polymorphism. A PCR-RFLP-based assay has been recently developed to rapidly identify isolates belonging to D. corticola or D. quercivora without the need for sequencing (Dreaden et al. 2014b). Given the virulence evidenced by artificial inoculation experiments on oak logs, D. quercivora represents a new serious risk for the health of cork oak forests (Linaldeddu et al. 2013).

      D. corticola infections limit both the vitality and the productivity of cork oak trees. The most common symptoms D. corticola causes on cork oak trees are sunken cankers on collar, trunk, and branches. These cankers often exude a dark brown sap, giving them the appearance of bleeding, which gradually dries to a blackish gluey mass on the bark (Fig. 2A). The wood becomes discolored and the vascular system necrotic. The symptoms’ appearance on the foliage (wilting) suggests that phytotoxic metabolites are involved in the host-pathogen interaction (Fig. 2B). Indeed, D. corticola is able to produce in vitro a broad array of secondary metabolites, some of which, including diplopyrone, diplofuranones A and B, diplobifuranylones A and B, and the SS-enantiomer of sapinofuranones B, C and D, show phytotoxic, antifungal, and antibacterial activities (Masi et al. 2016).

      Fig. 2.

      Fig. 2. Symptoms caused by Diplodia corticola on cork oak. A, trunk with necrosis and a black, mucilaginous exudate. B, wilting and death of shoots. C, acorn with erumpent pycnidia. D, particular of conidiogenous cells and conidia, bar = 12.5 µm.

      Download as PowerPoint

      Pycnidia of the fungus differentiate on all aerial tree organs infected, including acorns (Fig. 2C). Conidia (Fig. 2D) are dispersed by wind, water, or insect vectors. However, little is known about the inoculum potential, pattern of seasonal spore release, and abiotic factors favoring D. corticola infections in cork oak forests. Linaldeddu et al. (2010) found that natural infections of D. corticola on cork oak seedlings, exposed monthly for one year to the natural inoculum pressure of the pathogen in a declining cork oak forest, were variable during the year with two peaks of infections, one in May and one in September. Recently, it has been demonstrated that some wood-boring insects act as spore vectors for D. corticola. Inácio et al. (2011) found that the oak pinhole borer (Platypus cylindrus) is a vector of D. corticola which, together with some Raffaelea species, accounted for more than 90% of fungi present in the gut and in mycangia of this insect. More recently, Kostovcik et al. (2015) found that D. corticola is one of the fungi most frequently isolated from mycangia of two invasive insects: Xyleborus affinis and Xylosandrus crassiusculus, collected from various habitats across Florida. Interestingly, X. crassiusculus is considered a high-risk quarantine pest in Europe and has recently been reported from Italy (Pennacchio et al. 2003).

      Biscogniauxia mediterranea has emerged as an opportunistic and potentially invasive fungal pathogen. The frequency of its attacks on oaks has increased significantly over the past decades in the Mediterranean area. This increase in infection is associated with high mortality rate especially of young cork oak trees and it seems directly related to the increase in exceptionally dry and warm years (Desprez-Loustau et al. 2006; Henriques et al. 2012). Although several studies have demonstrated that B. mediterranea is less aggressive than D. corticola, it is the fungal species most commonly associated with declining oak trees especially during the final stage of the disease and contributes to accelerating tree decline and eventually tree death (Martín et al. 2005). The life cycle of B. mediterranea on cork oak includes first a latent endophytic phase, then a parasitic phase, and lastly a saprophytic phase (Franceschini et al. 2002). This fungus can persist as an endophyte in all of the aerial organs of cork oak trees. The endophytic behavior of B. mediterranea is influenced by changes in the host physiology with some stress factors, especially water stress, that can favor oak tissue colonization by this pathogen and promote its switch from an endophytic phase to a parasitic phase (Linaldeddu et al. 2011).

      B. mediterranea is a necrotrophic pathogen, whose infections induce extensive inner bark and xylem necrosis associated with blackish exudation from the outer bark. B. mediterranea produces several phytotoxic metabolites namely biscopyran, phenylacetic acid, and 5-methylmellein (Evidente et al. 2005). However, limited information is available on the specific role of these compounds in the development of disease symptoms. On infected tissues, the fungus develops the characteristic charcoal cankers (Fig. 3A).

      These cankers arise when the bark is torn by the black carbonaceous stromata exerting pressure in the ritidome. At that stage (saprophytic phase on dead tissues), B. mediterranea increases its biomass by producing great numbers of propagules (ascospores and conidia) that are easily dispersed by wind (Fig. 3B), water, and insects (Franceschini et al. 2002; Inácio et al. 2011). Precipitation (a period of three consecutive days with precipitation above 0.5 mm) is a crucial condition for ascospore release, whereas wind is the main way of dispersal (Henriques et al. 2014a). Several insects also contribute to the dispersal of this fungus in cork oak forests, their action being important not only as vectors of inoculum, but also because the wounds they cause can act as an infection point (Martín et al. 2005). The main insects known to be vectors of B. mediterranea are Agrilus spp., Platypus cylindrus, and Tropideres spp. (Inácio et al. 2011).

      Fig. 3.

      Fig. 3. Biscogniauxia mediterranea on cork oak. A, characteristic, black stromata (charcoal canker) erumpent through the bark. B, a sporulating canker on the lower trunk: spore masses, released in the form of a tan cloud, are dispersed by air currents.

      Download as PowerPoint

      B. mediterranea has been recently expanding its incidence, geographical distribution, and host range, proving to be an invasive pathogen favored by climate change (Desprez-Loustau et al. 2007; Jurc and Ogris 2006; Mirabolfathy et al. 2011; Ragazzi et al. 2012). The high level of genetic variability of this fungus might account for its plasticity and adaptability to variable environmental conditions (Henriques et al. 2014b).

      The list of invasive fungi of cork oak trees is increasing. In addition to B. mediterranea and D. corticola, new and “emerging” fungal pathogen include the canker agents Coryneum modonium (Bragança et al. 2013), Neofusicoccum parvum (Linaldeddu et al. 2007a), and several Ophiostomatoid fungi of the Raffaelea genus (Inácio et al. 2012).

      Root Pathogens

      Species in the genus Phytophthora (oomycetes) are arguably the most destructive root pathogens of cork oak. Since the early 1990s, Phytophthora cinnamomi has had a major impact in cork oak decline in Mediterranean European countries, including France, Italy, Spain, and Portugal (Brasier 1992; Robin et al. 1998; Scanu et al. 2013). Knowledge about the occurrence of the pathogen in western Africa is very scarce (Brasier 2003). The situation is in need of investigation, especially in view of the widespread distribution of cork oak in the region and of the recent report of P. cinnamomi on nursery plant material in Morocco (Touati et al. 2014).

      P. cinnamomi infects trees growing singly or in groups (Fig. 4A), invading the roots, collars, and trunks, from which a black exudate often oozes (Fig. 4B). Infected trees show extensive loss of both lateral, small, woody roots and fine roots. Consequently, the root system is hampered in absorbing and transporting water and nutrients, and this causes plant death. Slower growth is accompanied by leaf yellowing, microphyllia, crown thinning and development of epicormic shoots, usually followed by dieback of the entire tree (Camilo-Alves et al. 2013). Depending on the site and climate conditions, trees can die suddenly in one or two seasons, or exhibit a slow decline, which may occur for several years (Camilo-Alves et al. 2013). P. cinnamomi thrives in cork oak woodlands crossed by water courses, in lowlands with stagnant water, and wherever water abounds (Moreira and Martins 2005). Its successful propagation and dissemination is due to the production of a large number of zoospores, which are differentiated inside the sporangia and released in the soil water. Phytophthora zoospores are motile and are chemiotactically attracted to the roots, where they encyst and secrete a number of proteins that glue them to the root surface and facilitate the infection (Hardham and Cahill 2010).

      Fig. 4.

      Fig. 4. Symptoms caused by Phytophthora cinnamomi. A, sudden death of a group of mature cork oak trees. B, typical blackish exudates at the base of an infected cork oak tree.

      Download as PowerPoint

      The center of origin of P. cinnamomi is unknown, although Papua New Guinea seems the most likely center, given the high level of genetic diversity found among isolates of P. cinnamomi in this tropical region (Old et al. 1984). Although P. cinnamomi is probably native to tropical regions, this pathogen has become invasive in many Mediterranean areas characterized by prolonged and severe drought conditions (Shearer et al. 2004). This ecological adaption is due to the production of long-term survival structures, such as stromata-like hyphal aggregations, thick-walled chlamydospores, and selfed oospores on roots and root debris, enabling the pathogen to survive over unfavorable seasons such as the long, hot, and dry summers typical of Mediterranean ecosystems (Jung et al. 2013, 2016).

      Other Phytophthora species, namely P. quercina, P. gonapodyides, and P. psychrophila, have been recently associated with declining Mediterranean oaks in Italy and Spain and their pathogenicity has been demonstrated on Quercus faginea, Q. ilex, and Q. suber (Linaldeddu et al. 2014; Pérez-Sierra et al. 2013; Seddaiu et al. 2014).

      The oomycete Pythium spiculum was frequently isolated from declining cork oak roots and rhizosphere in southern Iberia (Serrano et al. 2012a). P. spiculum is often found simultaneously with P. cinnamomi in oak stands in southwestern Spain and southern Portugal. Owing to their different asexual reproductive structures and therefore soil water requirements, the two pathogens may be most active in different seasons and thus vicariant in pathogenicity, with a low level of competition between them for colonization of oak roots (De Vita et al. 2011).

      Other root pathogens of cork oak include Armillaria spp., which cause plant growth reduction, wood decay, and mortality (Marçais and Bréda 2006). The identification of Armillaria spp. was originally based on morphological traits and mating tests. Accurate DNA-based techniques were recently developed for identifying Armillaria species (Mulholland et al. 2012). Given the variable degrees of pathogenicity of Armillaria species (Sicoli et al. 2002), a fast and accurate identification of these taxa is crucial.

      Some species of Armillaria, like A. mellea, A. gallica, and A. tabescens, were found over the years to be important factors in the decline of oaks throughout Europe and North America (Brazee and Wick 2009; Marçais and Bréda 2006). However, reports of Armillaria infections on cork oak are sporadic (Bragança et al. 2004; Marras 1962b), and therefore the actual contribution of these pathogens to cork oak decline and mortality remains unresolved as does the true identity of the species involved.

      Cork Oak Forest Management: What to Do and What Not to Do

      Management options for cork oak forests should consider the specific economic, environmental, and social context, taking into account the characteristics of the forest and its ability to produce goods. Currently, the main cork oak goods correspond to the production of cork and occasionally firewood and acorns. Cork is extracted for the first time when the tree is 25 to 30 years old and about 60 cm in circumference at breast height, and thereafter usually at intervals of 9 to 10 years, though it can take up to 14 years for the cork on the trees to reach industrial size (Carvalho and Graça 2009). The effect of cork stripping on tree health has always been a concern for the sustainable management of cork oak forests (Correia et al. 1992). In addition to great water loss, cork stripping often causes dangerous wounds that represent the pathway for many fungi. In particular, extraction wounds act as a significant entry way for Diplodia corticola (Luque and Girbal 1989).

      Two studies conducted recently in Spain showed the effectiveness of benzimidazole fungicides (thiophanate-methyl and carbendazim) in reducing the incidence and severity of D. corticola cankers under field conditions (Luque et al. 2008; Serrano et al. 2015). However, the increasing restriction of fungicides for the control of fungal diseases in agriculture and forestry prompts an effort to identify new environmentally friendly control strategies. Promising results for the control of oak pathogens have been achieved in in vivo and in vitro bioassays using mutualistic endophytic fungi of the Trichoderma genus (Linaldeddu et al. 2007b). In particular, one endophytic strain of Trichoderma citrinoviride from cork oak was found to produce in liquid culture a mix of polypeptide antibiotics (peptaibols) that were very effective against seven forest tree pathogens, including D. corticola (Maddau et al. 2009).

      Trichoderma species have been extensively studied for their antagonistic properties (Howell 2003). However, only recently, attention has turned to endophytic Trichoderma species of woody plants with a high biocontrol potential (Mejía et al. 2008).

      Despite research efforts to find effective fungicide-based or biological control strategies, preventive measures should take priority in maintaining the health of cork oak trees. This both because cork oak stands are largely subjected to human activities—pesticide use is in these unique agroforestry systems a source of concern for the environment and the health of livestock and people—and because most of the above options for the control of D. corticola and the other fungi infecting wounds lack replication in different situations/areas to allow generalization and confidence about their effectiveness in the short- to medium-long term. Appropriate preventive measures would include: the extraction of cork to be carried out only by experienced personnel; an increase in the use of specific machines; the promotion of technical courses for cork extractors on the application of the best available techniques for minimizing tree wounds (Luciano and Franceschini 2006); and, finally, the promotion of training courses for stakeholders (plant owners, nursery personnel, foresters, etc.) on an integrated disease management of cork oak forests, requiring these special ecosystems a delicate balance between human needs and nature. All these strategies could help curtail infectious diseases and reduce and rationalize the use of chemical pesticides in cork oak stands.

      Cork oak stands vary widely in composition and density, and these two variables directly influence the impact and spread of diseases caused by the Pythiaceae (Phytophthora and Pythium). In Sardinia (Italy) and northeastern Spain, cork oak grows in pure or mixed stands or in closed forests with a density of 600 to 1,000 trees/ha whereas in Portugal and the rest of Spain it is often found in open, savanna-type woodlands (montado/dehesa) with a density of 40 to 160 trees/ha (Acácio et al. 2007). In the closed forests, the understory is less varied than in the open woodlands (Pérez-Ramos et al. 2008). The predominant shrubs of the understory are Arbutus unedo, Cistus spp., Crataegus monogyna, Erica spp., Myrtus communis, Lavandula spp., Phillyrea latifolia, Pistacia lentiscus, Rosmarinus officinalis, and Thymus spp., while grasses include mainly species such as Allium triquetrum, Asphodelus albus, Bellis sylvestris, Conopodium capillifolium, Galium aparine, and Scilla monophyllos (Pérez-Ramos et al. 2008). Some of these plant species were found to be infected with P. cinnamomi, although usually without showing disease symptoms. Species like Calluna vulgaris, Cistus spp., and Ulex spp. sometimes die due to root infection and Moreira and Martins (2005) suggested to use these species as indicators of the occurrence of P. cinnamomi in active disease sites. Mediterranean shrubs and grasses may provide an important basis for the production and survival of pathogen’s inoculum, thus acting as reservoirs for P. cinnamomi in infested sites. This was demonstrated for the leguminous Lupinus luteus commonly found in dehesa ecosystems in southern Spain (Serrano et al. 2010). Shrub clearing to facilitate cork extraction reduces understory composition and diversity (Pérez-Ramos et al. 2008), and this may have the indirect benefit of reducing P. cinnamomi attacks, as suggested for other Phytophthora species in Europe (Fichtner et al. 2011).

      Phytophthora diseases are exacerbated in cork oak stands simultaneously exploited for agriculture and grazing, as it often occurs in the sparse montado/dehesa (Camilo-Alves et al. 2013). Since grazing animals may be important vectors of Phytophthora species, grazing should be prohibited wherever these oomycetes are known or suspected to occur, especially at times when the soil is wet (Li et al. 2014). The eradication of root pathogens such as Phytophthora and Pythium species once they are established in a new environment is difficult, if not impossible, to achieve (Brasier 2008). For this reason, measures to mitigate the impact of these pathogens in cork oak stands should focus essentially on prevention/management and include: keeping people, pets, and grazing animals off contaminated areas; preventing, where possible, soil and water movement out of contaminated areas by means of suitable sewage control interventions; disinfecting shoes, tools, and vehicles that may have come in contact with contaminated soils; and using healthy plant material. The above strategies could be possibly combined, in some situations, with chemical and biological control. Recently, the use of calcium amendments and soil biofumigation with Brassica carinata commercial pellets proved effective in the control of P. cinnamomi infections in the dehesa agroforestry systems (Morales-Rodríguez et al. 2016; Serrano et al. 2012b). According to Fernández-Escobar et al. (1999), oak decline can be controlled by trunk injections with potassium phosphonate, which even at low concentrations triggers resistance. Phosphonate can also be applied as a soil drench, a leaf spray, or a trunk spray (Giblin et al. 2007).

      In order to provide an overview for ready and easy reference, serving also for those who are not plant health professionals, Table 1 summarizes the main preventive and/or curative measures against the most important pathogens of cork oak, grouped according to the tree organ on which they mainly occur. Readers wishing to find out more about specific topics should consult the literature cited.

      Table 1. The main pathogens of cork oak, with the symptoms they cause and recommended control measures

      Impact of Climate Change on Cork Oak Forests

      Global warming has become a common driver of forest decline worldwide (Allen et al. 2010). Climate change in the Mediterranean region is mainly characterized by a gradual rise in average temperatures plus an overall reduction in annual rainfall, which also becomes more irregularly distributed across the seasons and over the years, resulting often in extended drought periods (Giorgi and Lionello 2008).

      The changing climate may affect cork oak stands by modifying tree growth and mortality as well as cork production and quality (Besson et al. 2014; Carnicer et al. 2011; Oliveira et al. 2002). In particular, cork growth has been shown to be reduced by drought and high temperatures (Caritat et al. 2000). To maintain the economic and ecological value of cork oak woodlands under climate constraints, it is crucial to adopt adaptive management strategies. Palma et al. (2015) showed that adaptation of forest management by optimizing cork extraction schedule, reducing debarking surface, and increasing tree density could increase cork productivity under future climate change. However, given the heterogeneity of cork oak forests, the promotion of long term sustainable management practices and proactive measures based on afforestation efforts aimed at maintaining biodiversity and ecosystem services should be assessed at local or regional scale (Berrahmouni et al. 2009; Hidalgo et al. 2008).

      The change in climate not only affects cork oaks, but also many of the pathogens of cork oak, and the interaction of these pathogens with their host. However, different pathogens may be affected by climate change in very different ways, and hitherto our understanding of how particular pathogens are managing to adapt to climate change is limited (Desprez-Loustau et al. 2007).

      Temperature, rainfall, relative humidity, amount of light, leaf wetness, soil moisture, solar radiation, and air turbulence are just some of the variables affecting pathogen survival and infectivity. In southern Portugal and Spain, where the oomycete P. cinnamomi is a major factor in cork oak decline, it has been shown that the alternation of prolonged droughts and rainy periods, combined with adverse site conditions (infertile soils with lower levels of phosphorus, poorly drained soils) and a microclimate conducive to disease (e.g., stands located in south-facing hilly areas) create ideal conditions for the pathogen to thrive and deploy its virulence (Moreira and Martins 2005).

      Given the current projections for climate change, with increasing mean temperatures and frequency of climatic extremes such as drought, floods, and storms in Europe, a proliferation of Phytophthora root rots may be expected, thus increasing the instability and vulnerability of oak forest ecosystems (Brasier 1996). It has been predicted that increasing temperatures will lead to higher annual rates of survival for P. cinnamomi inoculum, resulting in a potential range expansion of the pathogen along the western coast of Europe of one to a few hundred kilometers eastward from the Atlantic coast within one century (Bergot et al. 2004).

      Moreover, strong physiological stress limits the vigor of trees and predisposes them to parasite attacks. Higher rates of infection by pathogenic endophytes such as B. mediterranea have been associated with cork oak decline when this is accompanied by persistent drought (Linaldeddu et al. 2011). The ecological impact of xylariaceous fungi has clearly increased in the Mediterranean area on several forest tree species in connection with exceptionally dry years (Desprez-Loustau et al. 2006; La Porta et al. 2008). Further research is needed to establish how higher temperatures and drought will affect the species-specific traits and population dynamics of a number of cork oak pathogens.


      In this review, we have analyzed the role of endemic and emerging pathogens that cause cork oak decline and mortality. Overall, there is a scarce literature on cork oak pathogens compared with other forest tree species. Studies in the last few decades on pathogenic members of the Phytophthora genus and of the Botryosphaeriaceae and Xylariaceae families have partially filled the gap. Moreover, research conducted in different countries in Africa, Europe, and North America has contributed to expanding knowledge about the pathogenicity, epidemiology, biology, invasiveness, and management of some of these pathogens in different oak forests (Dreaden et al. 2014a; Kostovcik et al. 2015; Linaldeddu et al. 2013; Lynch et al. 2013; Morales-Rodríguez et al. 2016; Moreira and Martins 2005; Serrano et al. 2015). Detailed and modern morphological descriptions coupled with DNA sequence data currently available in public databases are facilitating the identification of taxa (Martin et al. 2014; Phillips et al. 2013). Novel DNA-based diagnostics are contributing to a more rapid and accurate detection of pathogens from symptomatic and asymptomatic oak tissues (Moricca and Ragazzi 2000).

      The recent scientific evidence suggests that the theoretical model of Manion (1991) on the succession of events and factors (predisposing, inciting, and contributing) involved in oak decline cannot explain thoroughly the causes that drive the onset of the decline and mortality events. New findings emphasize how some emerging pathogens, many of which are endemic, may act synergistically to drive the rapid devastation of extensive oak ecosystems (Linaldeddu et al. 2014).

      These novel decline scenarios indicate that in the future only through a combined study of all the symptoms of oak trees (and not limited to those associated with a specific group of pathogens as has often been done in the past in which agents of root rot, cankers and dieback, and leaf diseases were studied separately on the basis of the specific skills of each researcher) will it be possible to achieve an accurate diagnosis of the phenomenon and consequently develop appropriate control strategies. In the same way, it will be important to consider that primary pathogens may themselves be affected directly by climate change and indirectly by host physiology adaptations.

      Literature Cited

      • Acácio, V., Holmgren, M., Jansen, P. A., and Schrotter, O. 2007. Multiple recruitment limitation causes arrested succession in Mediterranean cork oak systems. Ecosystems (N. Y.) 10:1220-1230. https://doi.org/10.1007/s10021-007-9089-9 CrossrefWeb of ScienceGoogle Scholar
      • Acácio, V., Holmgren, M., Rego, F., Moreira, F., and Mohren, G. M. J. 2009. Are drought and wildfires turning Mediterranean cork oak forests into persistent shrublands? Agrofor. Syst. 76:389-400. https://doi.org/10.1007/s10457-008-9165-y CrossrefWeb of ScienceGoogle Scholar
      • Aćimović, S. G., Harmon, C. L., Bec, S., Wyka, S., Broders, K., and Doccola, J. J. 2016. First report of Diplodia corticola causing decline of red oak (Quercus rubra) trees in Maine. Plant Dis. 100:649. LinkWeb of ScienceGoogle Scholar
      • Allen, C. D., Macalady, A. K., Chenchouni, H., Bachelet D., McDowell, N., Vennetier, M., Kitzberger, T., Rigling, A., Breshears, D. D., Hogg, E. H. T., Gonzalez, P., Fensham, R., Zhang, Z., Castro, J., Demidova, N., Lim, J. H., Allard, G., Running, S. W., Semerci, A., and Cobb, N. 2010. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For. Ecol. Manage. 259:660-684. CrossrefWeb of ScienceGoogle Scholar
      • Alves, A., Correia, A., Luque, J., and Phillips, A. J. L. 2004. Botryosphaeria corticola, sp. nov. on Quercus species, with notes and description of Botryosphaeria stevensii and its anamorph, Diplodia mutila. Mycologia 96:598-613. https://doi.org/10.2307/3762177 CrossrefWeb of ScienceGoogle Scholar
      • Alves, A., Linaldeddu, B. T., Deidda, A., Scanu, B., and Phillips, A. J. L. 2014. The complex of Diplodia species associated with Fraxinus and some other woody hosts in Italy and Portugal. Fungal Divers. 67:143-156. https://doi.org/10.1007/s13225-014-0282-9 CrossrefWeb of ScienceGoogle Scholar
      • Beccarisi, L., Biondi, E., Casavecchia, S., Ernandes, P., Medagli, P., and Zuccarello, V. 2010. La quercia da sughero (Quercus suber L.) nel Salento: analisi diacronica e sinfitosociologica (Adriatico meridionale, Italia). Fitosociologia 47:3-16. Google Scholar
      • Bergot, M., Cloppet, E., Pérarnaud, V., Déqué, M., Marçais, B., and Desprez-Loustau, M. L. 2004. Simulation of potential range expansion of oak disease caused by Phytophthora cinnamomi under climate change. Glob. Change Biol. 10:1539-1552. https://doi.org/10.1111/j.1365-2486.2004.00824.x CrossrefWeb of ScienceGoogle Scholar
      • Berrahmouni, N., Regato, P., Ellatifi, M., Daly-Hassen, H., Bugalho, M., Bensaid, S., Diáz, M., and Aronson, J. 2009. Ecoregional planning for biodiversity conservation. Pages 203-216 in: Cork Oak Woodlands on the Edge. Ecology, Adaptive Management and Restoration. J. Aronson, J. S. Pereira, and J. G. Pausas, eds. Island Press, Washington, DC. Google Scholar
      • Besson, C. K., Lobo-do-Vale, R., Rodrigues, M. L., Almeida, P., Herd, A., Grant, O. M., David, T. S., Schmidt, M., Otieno, D., Keenan, T. F., Gouveia, C., Mériaux, C., Chaves, M. M., and Pereira, J. S. 2014. Cork oak physiological responses to manipulated water availability in a Mediterranean woodland. Agric. For. Meteorol. 184:230-242. https://doi.org/10.1016/j.agrformet.2013.10.004 CrossrefWeb of ScienceGoogle Scholar
      • Blondel, J. 2006. The “design” of Mediterranean landscapes: a millennial story of humans and ecological systems during the historic period. Hum. Ecol. 34:713-729. https://doi.org/10.1007/s10745-006-9030-4 CrossrefWeb of ScienceGoogle Scholar
      • Bragança, H., Machado, H., Inácio, L., Henriques, J., Diogo, E., and Moreira, C. 2013. Detecção de Agentes Potencialmente Patogénicos em Sobreiro e Azinheira. In: Abstracts of the Congresso Florestal Nacional, Vila Real/Bragança, Portugal, 5-8 June 2013. Google Scholar
      • Bragança, H., Santos, N., and Tenreiro, R. 2004. Identification of Portuguese Armillaria isolates by classic mating-tests and amplified ribosomal DNA restriction analysis. Silva Lusitana 12:67-75. Google Scholar
      • Brasier, C. M. 1992. Oak tree mortality in Iberia. Nature 360:539. https://doi.org/10.1038/360539a0 CrossrefWeb of ScienceGoogle Scholar
      • Brasier, C. M. 1996. Phytophthora cinnamomi and oak decline in southern Europe. Environmental constraints including climate change. Ann. Sci. For. 53:347-358. CrossrefGoogle Scholar
      • Brasier, C. M. 2003. The role of Phytophthora pathogens in forests and semi-natural communities in Europe and Africa. Pages 6-13 in: Phytophthora Diseases of Forest Trees. E. M. Hansen and W. Sutton, eds. Forest Research Laboratory, Oregon State University, Corvallis, OR. Google Scholar
      • Brasier, C. M. 2008. The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathol. 57:792-808. https://doi.org/10.1111/j.1365-3059.2008.01886.x CrossrefWeb of ScienceGoogle Scholar
      • Brazee, N. J., and Wick, R. L. 2009. Armillaria species distribution on symptomatic hosts in northern hardwood and mixed oak forests in western Massachusetts. For. Ecol. Manage. 258:1605-1612. https://doi.org/10.1016/j.foreco.2009.07.016 CrossrefWeb of ScienceGoogle Scholar
      • Bugalho, M. N., Caldeira, M. C., Pereira, J. S., Aronson, J., and Pausas, J. G. 2011. Mediterranean cork oak savannas require human use to sustain biodiversity and ecosystem services. Front. Ecol. Environ 9:278-286. https://doi.org/10.1890/100084 CrossrefWeb of ScienceGoogle Scholar
      • Camilo-Alves, C. S. P., Clara, M. I. E., and Ribeiro, N. M. C. A. 2013. Decline of Mediterranean oak trees and its association with Phytophthora cinnamomi: a review. Eur. J. For. Res. 132:411-432. https://doi.org/10.1007/s10342-013-0688-z CrossrefWeb of ScienceGoogle Scholar
      • Campos, P., Daly-Hassen, H., and Ovando-Pol, P. 2007. Cork oak forest management in Spain and Tunisia: two case studies of conflicts between sustainability and private income. Int. For. Rev. 9:610-626. Web of ScienceGoogle Scholar
      • Campos, P., Ovando, P., and Montero, G. 2008. Does private income support sustainable agroforestry in Spanish dehesa? Land Use Policy 25:510-522. https://doi.org/10.1016/j.landusepol.2007.11.005 CrossrefWeb of ScienceGoogle Scholar
      • Caritat, A., Gutierrez, E., and Molinas, M. 2000. Influence of weather on cork-ring width. Tree Physiol. 20:893-900. https://doi.org/10.1093/treephys/20.13.893 CrossrefWeb of ScienceGoogle Scholar
      • Carnicer, J., Coll, M., Ninyerola, M., Pons, X., Sánchez, G., and Peñuelas, J. 2011. Widespread crown condition decline, food web disruption, and amplified tree mortality with increased climate change-type drought. Proc. Natl. Acad. Sci. USA 108:1474-1478. https://doi.org/10.1073/pnas.1010070108 CrossrefWeb of ScienceGoogle Scholar
      • Carvalho, M. A. S., and Graça, J. A. R. 2009. Cork bottle stoppers and other cork products. Pages 59-69 in: Cork Oak Woodlands on the Edge. Ecology, Adaptive Management and Restoration. J. Aronson, J. S. Pereira, and J. G. Pausas, eds. Island Press, Washington, DC. Google Scholar
      • Correia, O. A., Oliveira, G., Martins-Loução, M. A., and Catarino, F. M. 1992. Effects of bark-stripping on the water relations of Quercus suber L. Sci. Gerund. 18:195-204. Google Scholar
      • Costa, A., Madeira, M., Santos, J. L., and Oliveira, A. 2011. Change and dynamics in Mediterranean evergreen oak woodlands landscapes of southwestern Iberian peninsula. Landsc. Urban Plan. 102:164-176. https://doi.org/10.1016/j.landurbplan.2011.04.002 CrossrefWeb of ScienceGoogle Scholar
      • Costa, A., Pereira, H., and Madeira, M. 2010. Analysis of spatial patterns of oak decline in cork oak woodlands in Mediterranean conditions. Ann. For. Sci. 67:204. https://doi.org/10.1051/forest/2009097 CrossrefWeb of ScienceGoogle Scholar
      • De Vita, P., Serrano, M. S., Belbahri, L., García, L. V., Ramo, C., and Sánchez, M. E. 2011. Germination of hyphal bodies of Pythium spiculum isolated from declining cork oaks at Doñana National Park (Spain). Phytopathol. Mediterr. 50:478-481. Web of ScienceGoogle Scholar
      • Desprez-Loustau, M. L., Marcais, B., Nageleisen, L. M., Piou, D., and Vannini, A. 2006. Interactive effects of drought and pathogens in forest trees. Ann. For. Sci. 63:597-612. https://doi.org/10.1051/forest:2006040 CrossrefWeb of ScienceGoogle Scholar
      • Desprez-Loustau, M. L., Robin, C., Reynaud, G., Déqué, M., Badeau, V., Piou, D., Husson, C., and Marçais, B. 2007. Simulating the effects of a climate-change scenario on the geographical range and activity of forest pathogenic fungi. Can. J. Plant Pathol. 29:101-120. https://doi.org/10.1080/07060660709507447 CrossrefWeb of ScienceGoogle Scholar
      • Dreaden, T. J., Black, A. W., Mullerin, S., and Smith, J. A. 2014a. First report of Diplodia quercivora causing shoot dieback and branch cankers on live oak (Quercus virginiana) in the United States. Plant Dis. 98:282. https://doi.org/10.1094/PDIS-07-13-0736-PDN LinkWeb of ScienceGoogle Scholar
      • Dreaden, T. J., Davis, J. M., Wingfield, M. J., and Smith, J. A. 2014b. Development of a PCR-RFLP based detection method for the oak pathogens Diplodia corticola and D. quercivora. Plant Health Prog. https://doi.org/10.1094/PHP-RS-13-0122 LinkGoogle Scholar
      • Dreaden, T. J., Shin, K., and Smith, J. A. 2011. First report of Diplodia corticola causing branch cankers on live oak (Quercus virginiana) in Florida. Plant Dis. 95:1027. https://doi.org/10.1094/PDIS-02-11-0123 LinkWeb of ScienceGoogle Scholar
      • Evidente, A., Andolfi, A., Maddau, L., Franceschini, A., and Marras, F. 2005. Biscopyran, a phytotoxic hexasubstituted pyranopyran produced by Biscogniauxia mediterranea, a fungus pathogen of cork oak. J. Nat. Prod. 68:568-571. https://doi.org/10.1021/np049621m CrossrefWeb of ScienceGoogle Scholar
      • Fernández-Escobar, R., Gallego, F. J., Benlloch, M., Membrillo, J., Infante, J., and Pérez de Algaba, A. 1999. Treatment of oak decline using pressurized injection capsules of antifungal materials. Eur. J. Plant Pathol. 29:29-38. https://doi.org/10.1046/j.1439-0329.1999.00127.x CrossrefWeb of ScienceGoogle Scholar
      • Fichtner, E. J., Rizzo, D. M., Kirk, S. A., Webber, J. F., and Holt, A. 2011. Root infections may challenge management of invasive Phytophthora spp. in U.K. woodlands. Plant Dis. 95:13-18. https://doi.org/10.1094/PDIS-03-10-0236 LinkWeb of ScienceGoogle Scholar
      • Franceschini, A., Corda, P., Maddau, L., and Marras, F. 1999. Observations sur Diplodia mutila, pathogene du chêne-liege en Sardaigne. IOBC WPRS Bull. 22:5-12. Google Scholar
      • Franceschini, A., Maddau, L., and Marras, F. 2002. Osservazioni sull’incidenza di funghi endofiti associati al deperimento di Quercus suber e Q. pubescens. Pages 313-325 in: L’endofitismo di funghi e batteri patogeni in piante arboree e arbustive. A. Franceschini and F. Marras, eds. Carlo Delfino Editore, Sassari, Italy. Google Scholar
      • Franceschini, A., Marras, F., and Sechi, C. 1993. Funghi segnalati sulla Quercia da sughero (Quercus suber L.). Collana biologica N° 3. Stazione Sperimentale del Sughero, Tempio Pausania, Italy. Google Scholar
      • Giblin, F., Pegg, K., Thomas, G., Whiley, A., Anderson, J., and Smith, L. 2007. Phosphonate trunk injections and bark sprays. In: Proceedings of Sixth World Avocado Congress (Actas VI Congreso Mundial del Aguacate) 12-16 November 2007. Viña Del Mar, Chile. Google Scholar
      • Giorgi, F., and Lionello, P. 2008. Climate change projections for the Mediterranean region. Global Planet. Change 63:90-104. https://doi.org/10.1016/j.gloplacha.2007.09.005 CrossrefWeb of ScienceGoogle Scholar
      • Goncalves, E. 2000. The Cork Report. Bedfordshire, England, RSPB: 34. Google Scholar
      • Gonthier, P., Gennaro, M., and Nicolotti, G. 2006. Effects of water stress on the endophytic mycota of Quercus robur. Fungal Divers. 21:69-80. Web of ScienceGoogle Scholar
      • Hardham, A. R., and Cahill, D. M. 2010. The role of oomycete effectors in plant-pathogen interactions. Funct. Plant Biol. 37:919-925. https://doi.org/10.1071/FP10073 CrossrefWeb of ScienceGoogle Scholar
      • Hecht-Poinar, E. I., and Parmeter, J. R. 1986. Cryptocline cinerescens and Discula quercina causing twig blight of oaks in California. Plant Dis. 70:800. https://doi.org/10.1094/PD-70-800d CrossrefWeb of ScienceGoogle Scholar
      • Henriques, J., Barrento, M. J., Bonifacio, L., Gomes, A. A., Lima, A., and Sousa, E. 2014a. Factors affecting the dispersion of Biscogniauxia mediterranea in Portuguese cork oak stands. Silva Lusitana 22:83-97. Google Scholar
      • Henriques, J., Inácio, M. L., Lima, A., and Sousa, E. 2012. New outbreaks of charcoal canker on young cork oak trees in Portugal. IOBC WPRS Bull. 76:85-88. Google Scholar
      • Henriques, J., Nóbrega, F., Sousa, E., and Lima, A. 2014b. Diversity of Biscogniauxia mediterranea within single stromata on cork oak. J. Mycol. https://doi.org/10.1155/2014/324349 CrossrefGoogle Scholar
      • Hidalgo, P. J., Marín, J. M., Quijada, J., and Moreira, J. M. 2008. A spatial distribution model of cork oak (Quercus suber) in southwestern Spain: A suitable tool for reforestation. For. Ecol. Manage. 255:25-34. https://doi.org/10.1016/j.foreco.2007.07.012 CrossrefWeb of ScienceGoogle Scholar
      • Howell, C. R. 2003. Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis. 87:4-10. https://doi.org/10.1094/PDIS.2003.87.1.4 LinkWeb of ScienceGoogle Scholar
      • Inácio, M. L., Henriques, J., Guerra-Guimaraes, L., Gil Azinheira, H., Lima, A., and Sousa, E. 2011. Platypus cylindrus Fab. (Coleoptera: Platypodidae) transports Biscogniauxia mediterranea, agent of cork oak charcoal canker. Bol. Sanid. Veg., Plagas 37:181-186. Google Scholar
      • Inácio, M. L., Henriques, J., Lima, A., and Sousa, E. 2012. Ophiostomatoid fungi associated with cork oak mortality in Portugal. Integrated Protection in Oak Forests. IOBC WPRS Bull. 76:89-92. Google Scholar
      • Jung, T., Colquhoun, I. J., and Hardy, G. E. S. J. 2013. New insights into the survival strategy of the invasive soilborne pathogen Phytophthora cinnamomi in different natural ecosystems in Western Australia. For. Pathol. 43:266-288. CrossrefWeb of ScienceGoogle Scholar
      • Jung, T., Orlikowski, L., Henricot, B., Abad-Campos, P., Aday, A. G., Aguín Casal, O., Bakonyi, J., Cacciola, S. O., Cech, T., Chavarriaga, D., Corcobado, T., Cravador, A., Decourcelle, T., Denton, G., Diamandis, S., Dogmus-Lehtijärvi, H. T., Franceschini, A., Ginetti, B., Glavendekic, M., Hantula, J., Hartmann, G., Herrero, M., Ivic, D., Horta Jung, M., Lilja, A., Keca, N., Kramarets, V., Lyubenova, A., Machado, H., Magnano di San Lio, G., Mansilla Vázquez, P. J., Marçais, B., Matsiakh, I., Milenkovic, I., Moricca, S., Nagy, Z. Á., Nechwatal, J., Olsson, C., Oszako, T., Pane, A., Paplomatas, E. J., Pintos Varela, C., Prospero, S., Rial Martínez, C., Rigling, D., Robin, C., Rytkönen, A., Sánchez, M. E., Scanu, B., Schlenzig, A., Schumacher, J., Slavov, S., Solla, A., Sousa, E., Stenlid, J., Talgø, V., Tomic, Z., Tsopelas, P., Vannini, A., Vettraino, A. M., Wenneker, M., Woodward, S., and Peréz-Sierra, A. 2016. Widespread Phytophthora infestations in European nurseries put forest, semi-natural and horticultural ecosystems at high risk of Phytophthora diseases. For. Pathol. 46:134-163. https://doi.org/10.1111/efp.12239 CrossrefWeb of ScienceGoogle Scholar
      • Jurc, D., and Ogris, N. 2006. First reported outbreak of charcoal disease caused by Biscogniauxia mediterranea on Turkey oak in Slovenia. Plant Pathol. 55:299. Web of ScienceGoogle Scholar
      • Kostovcik, M., Bateman, C. C., Kolařík, M., Stelinski, L. L., Jordal, B. H., and Hulcr, J. 2015. The ambrosia symbiosis is specific in some species and promiscuous in others: evidence from community pyrosequencing. ISME J. 9:126-138. https://doi.org/10.1038/ismej.2014.115 CrossrefWeb of ScienceGoogle Scholar
      • La Porta, N., Capretti, P., Thomsen, I. M., Kasanen, R., Hietala, A. M., and Von Weissenberg, K. 2008. Forest pathogens with higher damage potential due to climate change in Europe. Can. J. Plant Pathol. 30:177-195. https://doi.org/10.1080/07060661.2008.10540534 CrossrefWeb of ScienceGoogle Scholar
      • Li, A. Y., Williams, N., Fenwick, S. G., Hardy, G. E. S. J., and Adams, P. J. 2014. Potential for dissemination of Phytophthora cinnamomi by feral pigs via ingestion of infected plant material. Biol. Invasions 16:765-774. https://doi.org/10.1007/s10530-013-0535-7 CrossrefWeb of ScienceGoogle Scholar
      • Linaldeddu, B. T., Franceschini, A., Alves, A., and Phillips, A. J. L. 2013. Diplodia quercivora sp. nov.: a new species of Diplodia on declining Quercus canariensis trees in Tunisia. Mycologia 105:1266-1274. https://doi.org/10.3852/12-370 CrossrefWeb of ScienceGoogle Scholar
      • Linaldeddu, B. T., Franceschini, A., Luque, J., and Phillips, A. J. L. 2007a. First report of canker disease caused by Botryosphaeria parva on cork oak trees in Italy. Plant Dis. 91:324. https://doi.org/10.1094/PDIS-91-3-0324A LinkWeb of ScienceGoogle Scholar
      • Linaldeddu, B. T., Hasnaoui, F., and Franceschini, A. 2009a. First report of Botryosphaeria corticola affecting Quercus afares and Q. canariensis in Tunisia. J. Plant Pathol. 91:234. Web of ScienceGoogle Scholar
      • Linaldeddu, B. T., Maddau, L., and Franceschini, A. 2007b. Attività antagonistica di isolati endofitici di Trichoderma spp. verso Botryosphaeriaceae associate al deperimento della quercia da sughero. Micol. Ital. 36:22-29. Google Scholar
      • Linaldeddu, B. T., Maddau, L., and Franceschini, A. 2010. Nuove acquisizioni su aspetti epidemiologici del patosistema Quercus suber/Botryosphaeria corticola in Sardegna. Micol. Ital. 39:49-57. Google Scholar
      • Linaldeddu, B. T., Scanu, B., Maddau, L., and Franceschini, A. 2014. Diplodia corticola and Phytophthora cinnamomi: the main pathogens involved in holm oak decline on Caprera Island (Italy). For. Pathol. 44:191-200. CrossrefWeb of ScienceGoogle Scholar
      • Linaldeddu, B. T., Sirca, C., Spano, D., and Franceschini, A. 2009b. Physiological responses of cork oak and holm oak to infection by fungal pathogens involved in oak decline. For. Pathol. 39:232-238. CrossrefWeb of ScienceGoogle Scholar
      • Linaldeddu, B. T., Sirca, C., Spano, D., and Franceschini, A. 2011. Variation of endophytic cork oak-associated fungal communities in relation to plant health and water stress. For. Pathol. 41:193-201. CrossrefWeb of ScienceGoogle Scholar
      • Luciano, P., and Franceschini, A. 2006. Ricerca e Sughericoltura. Composita sas, Sassari, Italy. Google Scholar
      • Luque, J., and Girbal, J. 1989. Dieback of cork oak (Quercus suber) in Catalonia (NE Spain) caused by Botryosphaeria stevensii. Eur. J. Forest Pathol. 19:7-13. https://doi.org/10.1111/j.1439-0329.1989.tb00764.x CrossrefWeb of ScienceGoogle Scholar
      • Luque, J., Parladé, J., and Pera, J. 2000. Pathogenicity of fungi isolated from Quercus suber in Catalonia (NE Spain). For. Pathol. 30:247-263. CrossrefWeb of ScienceGoogle Scholar
      • Luque, J., Pera, J., and Parladé, J. 2008. Evaluation of fungicides for the control of Botryosphaeria corticola on cork oak in Catalonia (NE Spain). For. Pathol. 38:147-155. CrossrefWeb of ScienceGoogle Scholar
      • Lynch, S. C., Eskalen, A., Zambino, P. J., Mayorquin, J. S., and Wang, D. H. 2013. Identification and pathogenicity of Botryosphaeriaceae species associated with coast live oak (Quercus agrifolia) decline in southern California. Mycologia 105:125-140. https://doi.org/10.3852/12-047 CrossrefWeb of ScienceGoogle Scholar
      • Maddau, L., Cabras, A., Franceschini, A., Linaldeddu, B. T., Crobu, S., Roggio, T., and Pagnozzi, D. 2009. Occurrence and characterization of peptaibols from Trichoderma citrinoviride, an endophytic fungus of cork oak, using electrospray ionization quadrupole time-of-flight mass spectrometry. Microbiology 155:3371-3381. Google Scholar
      • Maddau, L., Perrone, C., Andolfi, A., Spanu, E., Linaldeddu, B. T., and Evidente, A. 2011. Phytotoxins produced by the oak pathogen Discula quercina. For. Pathol. 41:85-89. Google Scholar
      • Manion, P. D. 1991. Tree disease concepts, 2nd Ed. Prentice-Hall, Englewood Cliffs, NJ. Google Scholar
      • Marañón, T., Ajbilou, R., Ojeda, F., and Arroyo, J. 1999. Biodiversity of woody species in oak woodlands of southern Spain and northern Morocco. For. Ecol. Manage. 115:147-156. https://doi.org/10.1016/S0378-1127(98)00395-8 CrossrefWeb of ScienceGoogle Scholar
      • Marçais, B., and Bréda, N. 2006. Role of an opportunistic pathogen in the decline of stressed oak trees. J. Ecol. 94:1214-1223. https://doi.org/10.1111/j.1365-2745.2006.01173.x CrossrefWeb of ScienceGoogle Scholar
      • Marçais, B., and Desprez-Loustau, M. L. 2014. European oak powdery mildew: impact on trees, effects of environmental factors, and potential effects of climate change. Ann. For. Sci. 71:633-642. https://doi.org/10.1007/s13595-012-0252-x CrossrefWeb of ScienceGoogle Scholar
      • Marras, F. 1962a. Contributi alla patologia della quercia da sughero (Quercus suber L.). Malattie fogliari causate da funghi parassiti in Sardegna. Memorie della Stazione Sperimentale del Sughero, Tempio Pausania, Italy. Google Scholar
      • Marras, F. 1962b. Contributi alla patologia della quercia da sughero (Quercus suber L.). Il “marciume radicale” causato da Armillaria mellea (Vahl). Quél. Memorie della Stazione Sperimentale del Sughero, Tempio Pausania, Italy. Google Scholar
      • Martin, F. N., Blair, J. E., and Coffey, M. D. 2014. A combined mitochondrial and nuclear multilocus phylogeny of the genus Phytophthora. Fungal Genet. Biol. 66:19-32. https://doi.org/10.1016/j.fgb.2014.02.006 CrossrefWeb of ScienceGoogle Scholar
      • Martín, J., Cabezas, J., Buyolo, T., and Patón, D. 2005. The relationship between Cerambyx spp. damage and subsequent Biscogniauxia mediterranum infection on Quercus suber forests. For. Ecol. Manage. 216:166-174. https://doi.org/10.1016/j.foreco.2005.05.027 CrossrefWeb of ScienceGoogle Scholar
      • Masi, M., Maddau, L., Linaldeddu, B. T., Cimmino, A., D’Amico, W., Scanu, B., Evidente, M., Tuzi, A., and Evidente, A. 2016. Bioactive secondary metabolites produced by the oak pathogen Diplodia corticola. J. Agric. Food Chem. 64:217-225. https://doi.org/10.1021/acs.jafc.5b05170 CrossrefWeb of ScienceGoogle Scholar
      • Mejía, L. C., Rojas, E. I., Maynard, Z., Van Bael, S., Arnold, A. E., Hebbar, P., Samuels, G. J., Robbins, N., and Herre, E. A. 2008. Endophytic fungi as biocontrol agents of Theobroma cacao pathogens. Biol. Control 46:4-14. https://doi.org/10.1016/j.biocontrol.2008.01.012 CrossrefWeb of ScienceGoogle Scholar
      • Mirabolfathy, M., Groenewald, J. Z., and Crous, P. W. 2011. The occurrence of charcoal disease caused by Biscogniauxia mediterranea on chestnut leaved oak (Quercus castaneifolia) in Golestan forests of Iran. Plant Dis. 95:876. https://doi.org/10.1094/PDIS-03-11-0153 LinkWeb of ScienceGoogle Scholar
      • Morales-Rodríguez, C., Vettraino, A. M., and Vannini, A. 2016. Efficacy of biofumigation with Brassica carinata commercial pellets (BioFence) to control vegetative and reproductive structures of Phytophthora cinnamomi. Plant Dis. 100:324-330. https://doi.org/10.1094/PDIS-03-15-0245-RE LinkWeb of ScienceGoogle Scholar
      • Moreira, A. C., and Martins, J. M. S. 2005. Influence of site factors on the impact of Phytophthora cinnamomi in cork oak stands in Portugal. For. Pathol. 35:145-162. CrossrefWeb of ScienceGoogle Scholar
      • Moricca, S., Ginetti, B., and Ragazzi, A. 2012. Species and organ-specificity in endophytes colonizing healthy and declining Mediterranean oaks. Phytopathol. Mediterr. 51:587-598. Web of ScienceGoogle Scholar
      • Moricca, S., and Ragazzi, A. 2000. Molecular markers and oak decline: how new diagnostic techniques can be used to address this multifaceted problem. Pages 187-215 in: Decline of Oak Species in Italy: Problems and Perspectives. A. Ragazzi and I. Dellavalle, eds. Accademia Italiana di Scienze Forestali, Firenze, Italy. Google Scholar
      • Moricca, S., and Ragazzi, A. 2008. Fungal endophytes in Mediterranean oak forests: A lesson from Discula quercina. Phytopathology 98:380-386. https://doi.org/10.1094/PHYTO-98-4-0380 LinkWeb of ScienceGoogle Scholar
      • Moricca, S., and Ragazzi, A. 2011. The Holomorph Apiognomonia quercina/Discula quercina as a Pathogen/Endophyte in oak. Pages 47-66 in: Endophytes of Forest Trees: Biology, and Application. A. M. Pirttila and A. C. Frank, eds. Forestry Sciences 80, Springer Science + Business Media B.V., Dordrecht, Netherlands. CrossrefGoogle Scholar
      • Mulholland, V., MacAskill, G. A., Laue, B. E., Steele, H., Kenyon, D., and Green, S. 2012. Development and verification of a diagnostic assay based on EF-1α for the identification of Armillaria species in northern Europe. For. Pathol. 42:229-238. CrossrefWeb of ScienceGoogle Scholar
      • Old, K. M., Moran, G. F., and Bell, J. C. 1984. Isozyme variability among isolates of Phytophthora cinnamomi from Australia and Papua New Guinea. Can. J. Bot. 62:2016-2022. https://doi.org/10.1139/b84-274 CrossrefWeb of ScienceGoogle Scholar
      • Oliveira, G., Martins-Loucao, M. A., and Correia, O. 2002. The relative importance of cork harvesting and climate for stem radial growth of Quercus suber L. Ann. For. Sci. 59:439-443. https://doi.org/10.1051/forest:2002018 CrossrefWeb of ScienceGoogle Scholar
      • Palma, J. H. N., Paulo, J. A., Faias, S. P., Garcia-Gonzalo, J., Borges, J. G., and Tomé, M. 2015. Adaptive management and debarking schedule optimization of Quercus suber L. stands under climate change. Case study in Chamusca, Portugal. Reg. Environ. Change 15:1569-1580. https://doi.org/10.1007/s10113-015-0818-x CrossrefWeb of ScienceGoogle Scholar
      • Pennacchio, F., Roversi, P. F., Francardi, V., and Gatti, E. 2003. Xylosandrus crassiusculus (Motschulsky) a bark beetle new to Europe (Coleoptera Scolytidae). Redia (Firenze) 86:77-80. Google Scholar
      • Pérez-Ramos, I. M., Zavala, M. A., Marañón, T., Díaz-Villa, M. D., and Valladares, F. 2008. Dynamics of understory diversity following shrub-clearing of cork oak forests: A five-year study. For. Ecol. Manage. 255:3242-3253. https://doi.org/10.1016/j.foreco.2008.01.069 CrossrefWeb of ScienceGoogle Scholar
      • Pérez-Sierra, A., Lopez-García, C., Leon, M., García-Jimenez, J., Abad-Campos, P., and Jung, T. 2013. Previously unrecorded low-temperature Phytophthora species associated with Quercus decline in a Mediterranean forest in eastern Spain. For. Pathol. 43:331-339. CrossrefWeb of ScienceGoogle Scholar
      • Phillips, A. J. L., Alves, A., Abdollahzadeh, J., Slippers, B., Wingfield, M. J., Groenewald, J. Z., and Crous, P. W. 2013. The Botryosphaeriaceae: genera and species known from culture. Stud. Mycol. 76:51-167. https://doi.org/10.3114/sim0021 CrossrefWeb of ScienceGoogle Scholar
      • Picco, A. M., Angelini, P., Ciccarone, C., Franceschini, A., Ragazzi, A., Rodolfi, M., Varese, G. C., and Zotti, M. 2011. Biodiversity of emerging pathogenic and invasive fungi in plants, animals and humans in Italy. Plant Biosyst. 145:988-996. https://doi.org/10.1080/11263504.2011.633118 CrossrefWeb of ScienceGoogle Scholar
      • Pinto-Correia, T. 1993. Threatened landscape in Alentejo, Portugal: The Montado and other agro-silvo-pastoral systems. Landsc. Urban Plan. 24:43-48. https://doi.org/10.1016/0169-2046(93)90081-N CrossrefWeb of ScienceGoogle Scholar
      • Pinto-Correia, T. 2000. Future development in Portuguese rural areas: how to manage agricultural support for landscape conservation? Land Urb. Plan. 50:95-106. Google Scholar
      • Ragazzi, A., Ginetti, B., and Moricca, S. 2012. First report of Biscogniauxia mediterranea on English Ash in Italy. Plant Dis. 96:1694. https://doi.org/10.1094/PDIS-05-12-0442-PDN LinkWeb of ScienceGoogle Scholar
      • Ragazzi, A., and Moricca, S. 2012. Il patosistema “endofita/specie arborea forestale” ed i cambiamenti climatici: analisi di un caso di studio. Micol. Ital. 2-3:11-27. Google Scholar
      • Ragazzi, A., Moricca, S., Capretti, P., and Dellavalle, I. 1999. Endophytic presence of Discula quercina on declining Quercus cerris. J. Phytopathol. 147:437-440. https://doi.org/10.1111/j.1439-0434.1999.tb03847.x CrossrefWeb of ScienceGoogle Scholar
      • Ragazzi, A., Moricca, S., and Dellavalle, I. 2007a. Ruggini di piante arboree forestali ed ornamentali. Pàtron Editore, Bologna, Italy. Google Scholar
      • Ragazzi, A., Moricca, S., Dellavalle, I., and Turco, E. 2002. Variations in the pathogenicity of Apiognomonia quercina isolates from different hosts. J. Plant Dis. Prot. 109:578-588. Web of ScienceGoogle Scholar
      • Ragazzi, A., Turco, E., Marianelli, L., Dellavalle, I., and Moricca, S. 2007b. Disease gradient of the anthracnose agent Apiognomonia quercina in a natural oak stand. Phytopathol. Mediterr. 46:295-303. Web of ScienceGoogle Scholar
      • Ragazzi, A., Vagniluca, S., and Moricca, S. 1995. European expansion of oak decline: involved microrganisms and methodological approaches. Phytopathol. Mediterr. 34:207-226. Google Scholar
      • Robin, C., Desprez-Loustau, M. L., Capron, G., and Delatour, C. 1998. First record of Phytophtora cinnamomi on cork and holm oaks in France and evidence of pathogenicity. Ann. For. Sci. 55:869-883. https://doi.org/10.1051/forest:19980801 CrossrefWeb of ScienceGoogle Scholar
      • Saikkonen, K., Faeth, S. H., Helander, M., and Sullivan, T. J. 1998. Fungal endophytes: a continuum of interactions with host plants. Annu. Rev. Ecol. Syst. 29:319-343. https://doi.org/10.1146/annurev.ecolsys.29.1.319 CrossrefGoogle Scholar
      • Scanu, B., Linaldeddu, B. T., Franceschini, A., Anselmi, N., Vannini, A., and Vettraino, A. M. 2013. Occurrence of Phytophthora cinnamomi in cork oak forests in Italy. For. Pathol. 43:340-343. CrossrefWeb of ScienceGoogle Scholar
      • Schulz, B., and Boyle, C. 2005. The endophytic continuum. Mycol. Res. 109:661-686. https://doi.org/10.1017/S095375620500273X CrossrefWeb of ScienceGoogle Scholar
      • Seddaiu, S., Sechi, C., Linaldeddu, B. T., Franceschini, A., and Scanu, B. 2014. Comparative aggressiveness of Phytophthora spp. to Mediterranean oaks. IOBC WPRS Bull. 101:117-124. Google Scholar
      • Serrano, M. S., De Vita, P., Fernández-Rebollo, P., Coelho, A. C., Belbahri, L., and Sánchez, M. E. 2012a. Phytophthora cinnamomi and Pythium spiculum as main agents of Quercus decline in Southern Spain and Portugal. IOBC WPRS Bull. 76:97-100. Google Scholar
      • Serrano, M. S., De Vita, P., Fernández-Rebollo, P., and Sánchez Hernández, M. E. 2012b. Calcium fertilizers induce soil suppressiveness to Phytophthora cinnamomi root rot of Quercus ilex. Eur. J. Plant Pathol. 132:271-279. https://doi.org/10.1007/s10658-011-9871-6 CrossrefWeb of ScienceGoogle Scholar
      • Serrano, M. S., Fernández, P., De Vita, P., Carbonero, M. D., Trapero, A., and Sánchez, M. A. E. 2010. Lupinus luteus, a new host of Phytophthora cinnamomi in Spanish oak-rangelands ecosystems. Eur. J. Plant Pathol. 128:149-152. https://doi.org/10.1007/s10658-010-9652-7 CrossrefWeb of ScienceGoogle Scholar
      • Serrano, M. S., Romero, M. A., Jimenez, J. J., De Vita, P., Avila, A., Trapero, A., and Sanchez, M. E. 2015. Preventive control of Botryosphaeria canker affecting Quercus suber in southern Spain. Forestry 88:500-507. https://doi.org/10.1093/forestry/cpv016 CrossrefWeb of ScienceGoogle Scholar
      • Shearer, B. L., Crane, C. E., and Cochrane, A. 2004. Quantification of the susceptibility of the native flora of the South-West Botanical Province, Western Australia, to Phytophthora cinnamomi. Australas. J. Bot. 52:435-443. https://doi.org/10.1071/BT03131 CrossrefWeb of ScienceGoogle Scholar
      • Sicoli, G., Annese, V., De Gioia, T., and Luisi, N. 2002. Armillaria pathogenicity tests on oaks in southern Italy. J. Plant Pathol. 84:107-111. Web of ScienceGoogle Scholar
      • Touati, J., Chliyeh, M., El Asri, A., Ait Aguil, F., Selmaoui, K., Ouazzani Touhami, A., Benkirane, R., and Douira, A. 2014. First report of Phytophthora cinnamomi associated with decline of the Cypress plants (Cupressus sempervirens) in Morocco’s nurseries. Int. J. Recent Sci. Res. 5:855-860. Google Scholar
      • Tsopelas, P., Slippers, B., Gonou-Zagou, Z., and Wingfield, M. J. 2010. First report of Diplodia corticola in Greece on kermes oak (Quercus coccifera). Plant Pathol. 59:805. CrossrefWeb of ScienceGoogle Scholar

      Salvatore Moricca

      Salvatore Moricca is an associate professor in the Department of Agri-food Production and Environmental Sciences, Plant Pathology and Entomology Division, at the University of Florence, Italy. He received his Ph. D. from the same university. He has been involved in studying the role of fungal and oomycete pathogens in forest ecosystems, the etiology of complex diseases, and the biology and life-history traits of rust pathogens, from pathogenesis to in vitro culture. His research, teaching, and outreach programs focus on pathogen detection, surveillance, and control, with an emphasis on the bio-ecology of invasive species in forest stands in relation to anthropogenic disturbance and climate change. He served as an independent reviewer for research proposals submitted to European Commission and other international research funding agencies. He serves as editor for scientific journals and as deputy coordinator of the IUFRO 7.02.05 – “Rusts of forest trees” Working Group. He is a fellow of the American Phytopathological Society, the British Society for Plant Pathology, the Italian Society for Plant Pathology, and the Mediterranean Phytopathological Union.

      Benedetto Teodoro Linaldeddu

      Benedetto Linaldeddu is a research fellow at the Department of Agriculture, University of Sassari, Italy. He graduated in agricultural science from the University of Sassari in 2001 and received his Ph.D. in plant pathology from the University of Bari in 2006. His main areas of interest focus on new or unusual plant diseases caused by invasive pathogens belonging to Botryosphaeriaceae and Diatrypaceae families. This research has led to a significant expansion of scientific knowledge about the diversity, ecological impact, epidemiology, taxonomy, and phylogeny of these pathogens, including the description of several new species and evolutionary lineages. He was awarded the Antonio Ciccarone Prize in 2006 for his research in plant pathology by the Mediterranean Phytopathological Union.

      Beatrice Ginetti

      Beatrice Ginetti obtained her Ph.D. in agricultural microbial biotechnologies from the University of Florence at the Department of Agri-food Production and Environmental Sciences, Plant Pathology and Entomology Division, in 2013. She dealt with the identification and epidemiology of the introduced alder rust pathogen Melampsoridium hiratsukanum in the Italian Alps. She investigated the role and impact of fungal endophytes in the decline of forest tree species in urban parks and in natural areas. Her research currently focuses on the study of Phytophthora spp. in forests and in nurseries. She identified a number of Phytophthora species previously unreported from Italy, including the newly described Phytophthora acerina. Her current work spans from field inspection for pathogen detection and identification to accurate pathogen identification and classification in the laboratory by means of traditional and molecular methods.

      Bruno Scanu

      Dr. Bruno Scanu received his Ph.D. in plant pathology at the University of Sassari, Italy, in 2011, and is currently working as research fellow in the Division of Plant Pathology and Entomology of the same university. His research focuses primarily on forest tree diseases with particular emphasis on those caused by the oomycete genus Phytophthora. His interests include the ecology, pathology, taxonomy, and phylogeny of new and unusual Phytophthora species, their spread and impact on natural ecosystems, plantation forestry, horticulture, and plant production nurseries. His recent research involves the management and control of Phytophthora diseases in Mediterranean forests.

      Antonio Franceschini

      Antonio Franceschini is professor of plant pathology at the University of Sassari. He graduated in agricultural science from the University of Sassari in 1971. He is currently coordinator of the section “oak pathogenic fungi” of the working group “Integrated Protection in Oak Forest” of the International Organization for Biological Control (IOBC), West Palearctic Regional Section. His research activity focuses on the ecology, biology, and physiology of endophytic and pathogenic fungi, with particular emphasis on the species involved in the etiology of oak decline. More recently, his research activity has been addressed to the detection and identification of Phytophthora species in forests and nurseries in Sardinia, Italy. His research activity is documented by more than 200 scientific papers in national and international journals.

      Alessandro Ragazzi

      Alessandro Ragazzi is professor of Forest Pathology in the Department of Agri-food Production and Environmental Sciences, University of Florence, Italy, and past president of the degree course in tropical agricultural sciences. He is currently responsible for the Plant Pathology and Entomology Division of the above mentioned department, and serves as editor-in-chief of the Italian Journal of Mycology. His research and extension interests are in the biology and epidemiology of pine rusts, the biology of Botryosphaeria spp., the study of oak decline, and the assessment of the role of microorganisms (pathogens and endophytes) in the etiology of complex diseases. Recently, his interests have turned to the study of alien pathogens and the role of climate change.