Similarities and Differences Among Factors Affecting Complex Declines of Quercus spp., Olea europea, and Actinidia chinensis

Abstract

The decline of perennial plant species, including oak, olive, and kiwifruit, is a phenomenon currently observed in many areas of the world. In this review, such species are chosen precisely because, despite the differences in their botany, native distribution, and current utilization, they are all affected by significant global or local declines. An analysis of the main common causes involved could be useful for a better understanding of the phenomenon. Quercus species are impacted by “Chronic Oak Decline” (COD), “Sudden Oak Decline” (SOD), and “Acute Oak Decline” (AOD). In Italy, olive groves are severely damaged by “Olive Quick Decline Syndrome”, whereas kiwifruit orchards are struck by “Kiwifruit Vine Decline Syndrome” (KVDS). Among the abiotic inciting stressors, drought, warmer temperatures, and waterlogging, all within a climate change scenario, are involved in all declines described herein as well as in plant dysbiosis. The involvement of some aggressive phytopathogens is another common feature of all these declines. Oomycetes contribute to COD, SOD, and KVDS; Xylella fastidiosa subsp. pauca and Botryosphaeriaceae affect olive, and some enterobacteria are involved in AOD, all representing decisive contributing factors. These declines are quite complex, and a comprehensive approach is required to dissect all the facets involved. A better understanding of altered host–microbial community relationships can lead to a more tailored approach to understanding and managing declines. Maintaining tree resilience in a warmer Earth remains a primary goal to achieve for preserving both natural ecosystems and profitable crops.

1. Introduction

In some areas of the world, over the last few decades, we have faced severe declines that affect both native and cultivated plant species [1,2]. Some of these declining species have been introduced from ecologically diverse regions and, through refined and ad hoc agronomical techniques and genetic breeding, have been led to yield profitable crops [3]. Regarding trees, during the declining phase, each species exhibits some common and visible facets that depict an incipient general stress of the plant: the wilting of the leaves and the withering of the branches, often followed by the plant’s death. These symptoms can also affect domesticated and perennial vine species, such as grapevine and kiwifruit.

Generally, the declines of plant species have been framed within a context of incoming climatic, edaphic, and agronomic stressors, coupled with the damaging activities of insects and/or plant pathogens that disturb the physiological equilibrium of the tree. Manion’s “death spiral” and Sinclair’s “four concepts” are among the most accepted models for studying tree decline complexes, and they are especially applied to declines in forest trees [4,5,6]. According to these models, some predisposing, inciting, and contributing stress factors act on a specific site to provoke tree decline. The tree is predisposed to decline by some adverse stressors that usually act over the long term (i.e., soil compaction, poor soil fertility, improper land management), and consequently, its health begins to decline. Then, one or more stressors, typically acting over a shorter period but capable of recurring in subsequent years (i.e., recurring droughts, insect defoliators, frost, waterlogging), incite further decline; subsequently, various contributing factors (i.e., insects and pathogens) perpetuate the decline until tree death occurs. The complex of stressors can act sequentially, simultaneously, and synergistically, all leading to the plant’s final decline and death. However, determining which is the main stressor that initiates the predisposition of the plant to decline, or the temporal sequence of stressors, is not an easy task. In some cases, adverse climatic factors seem responsible for triggering tree collapse [7], while in other instances, pests and pathogens are deemed predominant in the decline [8]. Additionally, both specific edaphic factors [9] and inadequate agronomic techniques [10] can also play a significant role in these declines.

Despite the potential predominance of one or more factors, the decline of perennial plants is a complex phenomenon that deserves considerable effort to fully decipher. To analyze and provide insights for future studies, some declines currently affecting important crops or native tree species have been compared. The abiotic and biotic stress factors involved in the declines of oaks (Quercus spp.), olive (Olea europaea L.), and kiwifruit (Actinidia chinensis Planch.) have been assessed and discussed to highlight possible similarities and differences. Such species have been chosen precisely because, despite the differences in their botany, native distribution, and current utilization in forestry and agriculture, they are all affected by significant global or local declines.

Quercus represents an important plant genus widely found in various forest ecosystems around the world. In the Mediterranean Basin, this genus covers a land area of approximately 23 million hectares [11]. Olive is a valuable crop mainly distributed across the Mediterranean Basin, and the global production of olive oil for the 2023/24 crop year was estimated to be about 2.5 million tons, with Spain, Italy, Tunisia, Turkey, Greece, and Portugal as the primary producers [12]. Kiwifruit is one of the most valuable fruit crops, and the global production reached about 4.5 million tons in 2022, with China, New Zealand, Italy, Greece, Iran, and Chile as the leading producers [13].

It is noteworthy to observe that the declines affect both native trees growing or producing in their original environment (i.e., Quercus spp., olive) and a perennial vine introduced to Europe from Eastern Asia several decades ago (i.e., kiwifruit), which has managed to achieve high yields. In Europe, the initial oak decline dates to before the 2000s, although the phenomenon appears to have become more pronounced during the last two decades. Oak decline is primarily reported throughout Europe and in the U.S.A., although it has also been recorded in North Africa and Asia [14]. Declines in olive and kiwifruit are mainly occurring in Italy, where they appeared quite contemporaneously around 15 years ago. In recent years, the declines of oaks, olives, and kiwifruit have been extensively assessed to discover both the main causes and the relationships between different individual causes in determining the outcome of the decline. However, a thorough comparison of these apparently different declines has never been carried out. By following models that consider not just a single factor as the sole cause of tree decline [4,5,6], this brief review analyzes the main predisposing, inciting, and contributing factors involved in the declines of oak, olive, and kiwifruit.

To reveal similarities and differences among these declines, a thematic analysis of the past and recent literature related to oak, olive, and kiwifruit declines was conducted to highlight the main facets of each decline. Oak declines were analyzed by considering the different syndromes currently observed worldwide. Regarding olive and kiwifruit, the literature review was applied to the declines recently observed in Italy. The main studies that take into consideration various climatic factors affecting plant physiology and soil properties, pathogen occurrence and their epidemiology, insect activities, tree management, and their observed and potential relationships were assessed. The key similarities and differences are pointed out and discussed here to provide study topics for managing the complex declines that currently affect other wood species worldwide.

2. Oak Declines

Quercus spp. are affected by different kinds of decline worldwide. Based on the time course of the symptom’s appearance and progression, three different kinds of decline are observed: (a) “Chronic Oak Decline”, (b) “Sudden Oak Decline”, and (c) “Acute Oak Decline”.

2.1. Chronic Oak Decline

“Chronic Oak Decline” (COD) occurs in oak forests in Europe, as well as in North America, northern Africa, and Asia [14]. The first signs of COD were reported multiple times during the 1920s, 1940s–1950s, and 1980s [15]; over the last three decades, the phenomenon has seemed more pronounced [16]. Symptoms related to COD include leaf yellowing, microphyllia, crown transparency and defoliation, bud death, twig and branch dieback, epicormic sprouts on branches, bark cracking, exudates along the trunk, necrotic bark lesions at the collar level, root necrosis and suberization, and tree death. These symptoms do not necessarily occur at the same time on individual trees, although the presence of some of them clearly indicates the occurrence of a decline. Symptoms related to COD are displayed in Figure 1 and Figure 2. Many Quercus species are affected by COD in their natural distribution areas: Europe (Q. robur L., Q. ilex L., Q. suber L., Q. cerris L., Q. frainetto Ten., Q. coccinea Munchh., Q. petraea (Matt). Liebl., Q. pubescens Willd); North America (Q. velutina (Lamarck), Q. rubra L., Q. falcata Michx., Q. marilandica Munchh).; northern Africa (Q. suber L).; western and eastern Asia (Q. mongolica Fisch. ex Ledeb, Q. mongolica subsp. crispula (Blume) H. Ohashi, Q. dentata Thunb., Q. brantii Lindl.) [17,18,19]. COD is characterized by a significantly long time until final tree death, which can occur decades after the first appearance of symptoms [14]. During this time lapse, several stressors can intervene in the area, thus contributing to the tree’s decline.

The classical stressor spiral leading to tree death is always triggered by certain predisposing factors [4,5,6]. In the case of COD, the main stressors considered as predisposing factors include soil compaction, poor soil fertility, heavy metal soil pollution, the old age of the trees, and improper forest management (i.e., overgrazing, intensive land use, neglected coppicing) [20,21,22,23,24]. Such stressors may or may not act simultaneously in the same area, and depending on the specific characteristics of the area, each may have a different impact on the subsequent decline. These predisposing stressors may inhibit, in the long term, the oak’s natural ability to face and respond to other damaging agents. For example, soil compaction leads to deficiencies in soil aeration and respiration, which reduces fine root formation in oak species; a reduced root system is a cause of the diminished ability to counteract other stressors [25]. Additionally, in the case of low soil nutrient availability, the holm oak root system shifts to produce thicker root branches and significantly fewer fine rootlets, representing an energy-consuming adaptive strategy at the expense of foliage maintenance [26].

Severe droughts have remained a major inciting stressor that promotes forest decline, including COD [27,28,29,30]. Drought, defined as a shortage of precipitation and soil moisture, can currently be linked to climate change and global warming [31]. In addition to semi-arid areas, drought events are frequently recorded in many parts of the world, including regions characterized by a temperate or continental climate where oaks are widely distributed [32,33]. Particularly, the recurring drought events occurring in the same area for consecutive years have been fundamental in triggering COD [16,34,35]. For oaks, indeed, drought induces a significant reduction in growth and relevant changes in wood anatomical properties that lead to hydraulic dysfunctions [36]. Defoliation caused by the insect defoliator species, namely Tortrix viridiana L., Lymantria dispar L., and Operophtera brumata L., is another important inciting stressor related to COD [37,38]. A single intense defoliation event by T. viridiana resulted in a significant decrease in oak secondary growth (i.e., the increase in plant organs, including the roots, driven by the vascular and cork cambium) over two consecutive years [38]. The impact of insect defoliation can be greater for oaks that are growing during a drought event [39]. Despite possible future tree recovery, both drought and insect defoliation can impact oak growth, with reduced growth seen as an early warning signal of potential tree death [40].

Winter and spring frost can also be significant stressors, especially when they are particularly severe [41]. Spring frost causes defoliation that impacts the photosynthetic activity of the tree, which is partially balanced by the second cohort of leaves that sprout during late spring [42]. Winter frost can also provoke significant wood cracking that can be further colonized by pathogens [43]. Waterlogging (i.e., when the soil surface is flooded) and flooding (i.e., when the water stands above the soil surface) also predispose oak trees to a decline, especially in combination with the presence of soil pathogens [44]. Waterlogging and flooding can have a highly negative impact on the overall physiology of the tree by depriving oxygen from soil pores, leading to hypoxia and subsequently anoxia [45,46,47]. After sensing oxygen deficiency, the plant alters its metabolism, with alcoholic fermentation replacing mitochondrial respiration. The main consequence of waterlogging is the cessation of root respiration and the closure of the leaf stomata, leading to a decrease in gas exchange rates and, in turn, a decrease in photosynthetic activity [45,46,47]. Anaerobic conditions in the soil also lead to a shift in the microbial community and cause significant denitrification [48], resulting in the depletion of soil nitrogen content [49].

In some cases of COD, the virulent activity of certain pathogens is retained as a decisive contributing factor for the tree decline, so that for some of them, a major role as a causal agent rather than a final contributing factor is proposed. The oomycetes Phytophthora cinnamomi and P. quercina, mainly isolated from the tree rhizosphere, are the most aggressive pathogens that, upon pathogenicity tests, display virulence to the roots of some oak species: P. cinnamomi on Q. ilex and Q. suber in the Mediterranean areas and on Q. alba in eastern United States [50,51,52,53,54]; P. quercina on Quercus robur, Q. petraea, Q. cerris, Q. pubescens, Q. ilex in Central and Southern Europe as well as on Q. suber in Sardinia (Italy) [54,55]. It is noted that several Phytophthora species, except for P. cinnamomi, can also be isolated from rivers [54]. Additionally, some pathogenic Botryosphaeriaceae species, namely Botryosphaeria dothidea, B. obtusa, and B. parva as well as Biscogniauxia mediterranea and Diplodia corticola, have been isolated from Q. suber in Italy [56,57,58,59], whereas Gnomoniopsis quercicola, Neoscytalidium dimidiatum, and B. dothidea have been found to be pathogenic to Q. brantii in Iran [60], and Raffaelea quercus-mongolicae and R. quercivora have been found to be pathogenic to Q. mongolica in South Korea and Japan, respectively [19]. Such fungi can inherently exhibit pathogenic behavior toward oak species, even though a survey performed in France revealed that oak stands of Q. robur and Q. petraea did not show any signs of a decline despite a significant presence of P. quercina and other Phytophthora spp. in the soil [61]. Within this context, the influence of certain climatic events, such as rainy periods during spring and summer drought, has been considered very important in augmenting or diminishing the potential aggressiveness of P. cinnamomi [62]. The oomycete inoculum is indeed strongly favored by rainy periods that can occur during warm spring and is reduced in cases of summer drought [62]. Among other contributing factors that can affect COD are the wood and bark boring insects that are considered as additional stressors for declining trees [37,63]. Xylophagous insects, indeed, are attracted by such trees, and they can cause the death of the tree through their feeding and reproductive activities within the wood [64].

Figure 2. Field symptoms of Chronic Oak Decline (COD) as observed in Italy on Quercus suber (a–e). Phytophthora spp. are associated with these declines and are considered the main contributing factor for the decline. (Reproduced from Ref. [54]).

Figure 2. Field symptoms of Chronic Oak Decline (COD) as observed in Italy on Quercus suber (a–e). Phytophthora spp. are associated with these declines and are considered the main contributing factor for the decline. (Reproduced from Ref. [54]).

In this complex decline, the stressors described herein can often act either simultaneously or sequentially, thereby accelerating oak decline. An example of the cumulative negative effects caused by the simultaneous occurrence of a long-term predisposing factor and an inciting stressor has been observed in a declining Q. robur forest. In this case, the presence of heavy metals in the soil and their consequent translocation into the tree were accompanied by the occurrence of summer droughts, which significantly increased the rate of decline [65]. The subsequent presence of additional inciting stressors affecting the same oak stand can initiate COD. Two consecutive years of drought, indeed, can trigger a multidecadal period of decline, and during this time, other stressors, such as waterlogging, can promote the growth and aggressiveness of oomycetes on the root system [66]. A high soil nitrogen content can increase the prevalence of Phytophthora species [67], whereas the combination of excess soil nitrogen and drought has a pronounced impact on certain allelochemicals compared to nitrogen alone, resulting in a significant reduction in tannin concentrations in the leaves, thus increasing oak vulnerability to defoliators [68]. Drought can also enhance the activities of insect defoliators [69].

2.2. Sudden Oak Decline

“Sudden Oak Decline” (SOD) is also known as “Sudden Oak Death”. This decline has been reported in the U.S.A., specifically in coastal California and Oregon, mainly affecting Q. agrifolia, Q. kelloggii, Q. chrysolepis, and the tanoak (Lithocarpus densiflora). The decline was first observed in 1995, and the fungal-like water mold oomycete Phytophthora ramorum is regarded as the main causal agent of SOD [70,71]. The primary symptoms include initial bleeding on the trunk, branches and twigs followed by canker formation, and shoot tip wilting upon sprouting. The foliage is pale green, while the exudates are dark brown or amber colored. The symptoms are more pronounced in the basal part of the tree. The canker causes the death of the tree by girdling the trunk and branches [70,71]. Representative symptoms of SOD are shown in Figure 3 and Figure 4.

P. ramorum also causes tree diebacks in northern Europe (i.e., England and Ireland), mainly affecting Larix kaempferi, and it can infect more than 100 plant species, including Rhododendron spp. [72,73]. It is worth noting that this pathogen has most likely been introduced into both North America and Europa from Asia [72]. The time frame within which oaks infected by P. ramorum die can be quite rapid (i.e., two to three years) [74], even though the infective phase leading to the tree death can extend up to five years [73]. Dying trees are colonized and further damaged by the bark beetle Scolytus spp. and by the fungus Annulohypoxylon thouarsianum [74]. Epidemiological studies have confirmed that SOD has a primary inciting factor along with a contributing factor such as the virulent P. ramorum. However, the effective colonization of oaks by this oomycete is strongly favored by two key predisposing factors: an excess of spring rain in the area (i.e., rainfall higher than the 30-year average) coupled with warm temperatures (i.e., 20 °C) [73]. The occurrence of a nearby plant species that acts as a “spreader” of the oomycete inoculum (i.e., Umbellularia californica) is also another essential predisposing factor that facilitates the spread of the infection among the oaks [73]. P. ramorum is an effective colonizer of leaves, and leaf colonization is considered pivotal for the further infection of the stem [75]; its virulence is enhanced by an air temperature of 20 °C [75].

A link between SOD and wildfires, which frequently occur along the coasts of California, has been documented [76]. Upon the occurrence of fires in areas where SOD has caused the death of oak trees, it has indeed been observed that the increase in the accumulation of a coarse woody surface derived from fuels of dead trees decreases the likelihood of belowground survival for resprouting tanoak trees [76]. This is most likely due to a significant depletion of carbon and plant nutrients (i.e., nitrogen, calcium, phosphorus) that occurs after a wildfire [77]. In this ecosystem, wildfire appears to be an important predisposing factor for the further SOD of tanoak trees. Other predisposing and/or inciting stressors observed for COD, such as soil compaction, poor soil fertility, drought, frost, and waterlogging, are not mentioned for SOD [72,78].

2.3. Acute Oak Decline

“Acute Oak Decline” (AOD) was first described in the United Kingdom in 2014 [79]. Subsequently, it has also been reported in other European countries (i.e., Portugal, Spain, Slovakia, Switzerland, France, Italy, Poland, Latvia), primarily on Q. robur, Q. petraea, and Q. suber, but also on Q. rubra, Q. cerris, and Q. coccinea [24,80,81,82], as well as in western Asia (i.e., Iran) on Q. brantii and Q. castaneifolia [83]. The main symptoms include crown transparency, twig dieback, bark cracking accompanied by a sticky blackish exudate, extensive necrotic lesions under the bark, and the frequent occurrence of wood galleries induced by the larvae of the insect beetle Agrilus biguttatus [24,79]. Exudates occur during spring as well as in autumn. Symptoms related to AOD are displayed in Figure 5. Typically, the affected tree dies over 3–5 years after a period of reduced stem growth [24,79].

A series of predisposing stressors are considered involved in the AOD: low soil pH, low soil phosphorus and sulfur content, high soil aluminum and base cation content, higher nitrogen deposition, lower rainfall, warmer temperatures, and water saturation in soil [84,85,86]. Such stressors are retained as fundamental for predisposing the oak stands to the further and ultimate activities of bacteria and A. biguttatus [87]. Some enterobacteria, indeed, are consistently isolated from the bark lesions of declining oak trees, namely Brenneria goodwinii, Gibbsiella quercinecans, Rahnella victoriana, and Lonsdalea britannica [24]. These bacteria have also been found in asymptomatic oak trees growing in the same oak stands that host trees exhibiting visible symptoms of AOD [88]. Interestingly, these bacteria do not induce lesions when inoculated alone [88], so that necrotic lesions have been observed only when B. goodwinii has been co-inoculated with G. quercinecans, R. victoriana, or A. biguttatus eggs [89,90]. Extensive genomic studies have allowed for the postulation that this complex of bacteria is an opportunistic polyspecies that can incite relevant damage when some predisposing factors weaken the oak trees [90,91]. The bleeding cankers they incite along the trunk are a specific contributing facet of a broader scenario that leads to AOD [24]. It is noteworthy that B. goodwinii and G. quercinecans can also inhabit soil, leaf litter, acorns, catkins, buds, and water [92,93]. The activity of the larval beetle A. biguttatus inside the wood is considered another final contributing factor for the death of the oaks [94]. Moreover, the bacteria involved in AOD can also be isolated from the beetle larvae, and this association could potentially trigger the virulence of B. goodwinii through some chemical elicitor compound(s) that the larva excretes [24].

3. Olive Decline

The “Olive Quick Decline Syndrome” (OQDS) has been affecting the olive groves of Salento (Apulia, Italy) for about 15 years. The main symptoms attributed to OQDS are leaf, twig, and branch dieback, followed by tree death. No apparent symptoms are observed in the root system. Symptoms related to OQDS are displayed in Figure 6. The primary cause of this decline has been solely attributed to Xylella fastidiosa subsp. pauca sequence type 53 [95]; however, at the onset of the epidemic, a more complex scenario was proposed to explain the decline, including the involvement of fungi (i.e., Phaeoacremonium parasiticum, P. rubrigenum, P. aleophilum, P. alvesii, Pleruostomophora richardsiae, Neofusiccoccum mediterraneum, N. australe, N. vitifusiforme, and Phaeomoniella sp). and insects (i.e., Zeuzera pyrina), as outlined in [96].

However, by applying a more comprehensive approach that takes into consideration the stressors involved in the forest declines, other facets of the olive decline are emerging. The involvement of several decisive predisposing factors related to climate change all occurring in the areas of decline (i.e., droughts, higher temperatures, soil salinization, waterlogging, frost), along with some agronomic practices coupled with the widespread occurrence of relevant inciting/contributing factors (i.e., phytopathogenic fungi), is currently revealing a more intricate scenario similar to those pertaining to the oak declines [97]. Drought may have played a fundamental role in triggering OQDS. In July and August from 2007 to 2018, very low precipitation was recorded in the area of the first OQDS outbreak [98]. In this scenario, it should be noted that drought enhances the symptoms caused by X. fastidiosa in the infected plants [99,100]. Of relevant importance, it also induces a higher aggressiveness in Diplodia seriata, isolated from trees showing OQDS, toward olive [98]. Additionally, the same fungus, otherwise not particularly aggressive, is also triggered by high temperatures [98]. Drought and prolonged warm temperatures during summer may have also favored the virulence of N. mediterraneum [101]. This fungus has proven highly aggressive to olive plants being capable of killing them just two to three weeks after the inoculation [101], whereas X. f. subsp. pauca ST 53 causes only some twig dieback after more than one year from the inoculation [102]. In addition to N. mediterraneum, another thermophilic fungal species, N. stellenboschiana, is involved in the olive decline where OQDS occurs [103]. It is noteworthy that both fungal species have been observed as virulent regardless of the inoculation time (spring/summer and autumn/winter) [103]. It is also important to mention that these fungi were isolated from olive trees that also host X. f. subsp. pauca [98,101,103].

Recurrent droughts in Salento also incite the salinization of groundwater [104], thereby augmenting the risk possibly caused by an excess of salt content in the soil, which can, in turn, induce a reduction in the photosynthetic activity of the trees [105]. Waterlogging, frequently observed in the areas affected by OQDS, also quickly weakens olive trees and predisposes them to further pathogenic activities of microorganisms [97,105]. Some agronomic practices extended over decades in the olive groves may also have impacted the overall ability of the trees to face additional stressors. Among these, the excessive application of herbicides, regularly performed in the OQDS-affected area during the last decades [106], may have induced soil nutrient imbalances [107]. It is quite clear that a range of abiotic and biotic predisposing, inciting, and contributing stressors are acting in Salento against olive groves, leading to a more complicated scenario compared to that invoked as caused by a single pathogen (i.e., X. f. subsp. pauca) currently inciting the olive decline. However, the interplay that occurs among different stressors over the seasons and the years still needs to be fully elucidated.

4. Kiwifruit Vine Decline Syndrome

The “Kiwifruit Vine Decline Syndrome” (KVDS), also known as “Kiwifruit Early Decline Syndrome” or “Kiwifruit Decline”, has been affecting kiwifruit orchards in Italy for about 15 years, involving both the green-fleshed (A. chinensis var. deliciosa) and yellow-fleshed (A. chinensis var. chinensis) cultivars. The main symptoms of KVDS include leaf curling and wilting, followed by leaf drop, observed especially during summer, as well as twig wilting, extensive root decay accompanied by stele breakage and cortex detachment, and a significant reduction in the finer roots. Symptoms related to KVDS are shown in Figure 7. Once visibly apparent, the decline progresses rapidly, leading to the death of the entire orchard within a few weeks or months [108]. Several factors contribute to this decline, including both abiotic (i.e., waterlogging, high soil temperature) and biotic (i.e., oomycetes, fungi, bacteria) stressors, along with certain agronomic practices that lead to soil compaction (i.e., repeated use of tractors), all contributing to the decline.

An excess of water in the soil, which can arise from either overirrigation or waterlogging, largely exacerbated by soil compaction, most likely represents the foremost predisposing/inciting stressor that triggers a series of physiological disorders leading to ultimate KVDS [108]. It is noteworthy that this decline has also been reported in orchards where waterlogging rarely occurs or is prevented [108]. Kiwifruit is native of hilly areas of eastern and southern Asia [109] and has been acclimatized to yield outside these regions through refined agronomical techniques. Kiwifruit requires humidity for its growth [109], but the soil water content found in the areas characterized by the KVDS in Italy significantly exceeds that occurring naturally in wild environments [108]. The excess of waterlogging may be linked to climate change [110], and a direct connection between waterlogging and the involvement of certain phytopathogenic oomycetes, such as Phytopythium vexans and P. chamaehyphon, in causing the KVDS has also been established [111,112]. However, soil water content near field capacity also seems to trigger such pathogens and consequently KVDS [112]. Another consequence of climate change, in particular prolonged higher temperatures, may be the increase in soil temperature, especially noted during summer [113,114]. This repeated condition (i.e., soil temperature between 20 °C and 25 °C over three months) leads to a significant deterioration of the root system [113], and a remarkable hydraulic dysfunction was observed in the KVDS-affected plants following the rise in soil temperature [115]. A reduction in xylogenesis and xylem functionality, indeed, leads to vessel narrowing and cavitation, and xylem implosion, which, in turn, causes low stomatal conductance and a reduction in photosynthesis, predisposing the plant to a subsequent and quite rapid decline [115].

Oomycetes, fungi, and bacteria are implicated in KVDS and represent critical inciting/contributing factors to this syndrome. The oomycetes appear to be primarily involved, with Phytopythium spp. and Phytophthora spp. being the main groups frequently isolated from KVDS-affected orchards and proven to be pathogenic upon pathogenicity tests [111,112,116,117]. Desarmillaria tabescens, Fusarium spp., and Cylindrocarpon spp. were also consistently found on declining kiwifruit plants [116,118], as well as anaerobic bacteria belonging to Clostridium genus [119]. The emergence of such pathogens and/or opportunistic pathogens seems correlated with the occurrence of previously outlined abiotic stressors (i.e., excess of water in soil and elevated soil temperature), leading to the postulation of a clear multifactorial syndrome [118].

5. Declines and Dysbiosis

Within the emerging holobiont scenario (i.e., the growth and health of macroorganisms are influenced by complex microbial communities capable of regulating their functions) [120], there is evidence that microbial dysbiosis is a common feature occurring in declines of oak, olive, and kiwifruit. Microbial dysbiosis indicates a shift in soil and/or plant organ microbiota composition linked to abiotic or biotic stressors that affect the plant during a specific period [121]. Dysbiosis can reveal an overall altered response of the plant to such stressors [121]. It should be noted that the microbiota of a healthy plant comprises beneficial, neutral, and pathogenic members that coexist in a homeostatic phase within the same organ, thereby providing chemical signals for plant health and development [122]. Drought can affect physicochemical soil properties and, in turn, soil microbial communities by modifying their metabolism and survival rates, consequently leading to a reduction in nutrient availability that causes tree decline [123]. Regarding COD, it has been observed that the initial phase of Q. ilex decline in the “dehesa” ecosystem in Spain is linked to significant denitrification and phosphorus mineralization provided by an altered rhizosphere microbiota during drought and the consequent tree defoliation [124]. In this situation, the primary effect of the drought (i.e., tree defoliation) is followed by the secondary and fundamental consequences caused by the defoliation on the microbial community of the rhizosphere. A significant reduction in photosynthesis strongly influences the rhizosphere microbiota, which begins to diminish the nitrogen and phosphorus availability for the tree, thus promoting further decline [124]. Regarding AOD, there is also some evidence of dysbiosis in the rhizosphere of declining trees, which showed low pH and different microbial compositions compared to healthy trees [125]. In the OQDS, there is evidence of a diverse composition in the leaf petiole endophytic community between susceptible and tolerant cultivars; in this case, susceptible cultivars exhibited a significant reduction in beneficial microbes [126]. In KVDS-affected plants, a marked reduction of beneficial soil microbes, including those involved in nutrient cycling and pathogen suppression, has been observed [118,127]. Moreover, an overall altered microbial composition and diversity in the rhizosphere of KVDS-affected plants that varies across different seasons has also been verified [128]. Such dysbiosis points to higher β-glucosidase activity, possibly linked to the increased occurrence of oomycetes in KVDS-affected plants [128] and to a significant reduction in the nitrogen content available for plant [129].

6. Similarities and Differences Between Oak, Olive, and Kiwifruit Declines

The progression of events that led to the decline observed in Quercus spp., olive, and kiwifruit shows remarkable similarities and differences. All of them fit well into scenarios where predisposing, inciting, and contributing factors act, either in a temporal sequence or simultaneously, to trigger the initial phase of decline. In any case, the severity of the decline appeared more pronounced during the last few decades, and a direct link to the climate change conditions we are currently facing seems quite clear [130]. The main similarities and differences among the declines affecting oak, olive, and kiwifruit are displayed in Figure 8.

This situation indicates that drought and/or higher air and soil temperatures remain the primary stressors that initiate the tree crisis, thus acting as a decisive predisposing factor. Drought events, particularly if repeated, clearly determine the outcome of COD [28,30] and OQDS [100]. For SOD, higher temperatures are retained as a predisposing stressor [75], while temperature stress events leading to a significant reduction in tree growth can predispose the tree to AOD [85]. Regarding KVDS, where drought situations are impossible to observe due to the water supply needed for plant yield, the decline can be exacerbated by the occurrence of higher soil temperatures during summer, which impact the rhizosphere’s health and the xylem’s hydraulic functionality [113,115].

It is evident that such stress factors affect both naturally acclimated species like Quercus spp. and olive, as well as plant species brought to cultivation from ecologically different environments, such as kiwifruit assessed herein. It is worth noting that a single drought event can have a long-lasting negative impact on the overall physiology of the tree, as observed in oak species that largely grow in Europe (i.e., Q. petraea, Q. robur) [131]. Additionally, the period during which the drought occurs has a clear relationship with the possibility of the trees recovering. For Q. petraea and Q. robur, spring drought negatively affects tree vitality more than summer drought does [131]. It is not unusual for droughts to act simultaneously or in a strict sequence with other stressors, which considerably amplifies the magnitude of the negative effects. Drought and premature spring sprouting due to warm temperatures are recognized as decisive inciting stressors for COD [132]. Similarly, drought combined with defoliation causes a reduction in the hydraulic conductance of oak trees [133]. Drought can differentially activate genes related to water functions in different olive cultivars (i.e., Cellina di Nardò and Leccino), leading to varying outcomes in susceptibility to subsequent infections by X. f. subsp. pauca [134]. Drought can also incite embolism and cavitation within the xylem tissue of olive cultivars, facilitating the metabolic activity of the bacterium and the progression of the infection [135].

Waterlogging or an excess of soil water are other predisposing stressors common to all declines described herein. In addition, the occurrence of water saturation in the soil largely favors the further pathogenic activities of oomycetes involved in COD, SOD, and KVDS [50,71,118]. It is also important to emphasize that, in addition to the physiological damage that an excess of water can cause to the tree [45,46,47,48], a combination of two stressor events occurring at the same site, such as drought and waterlogging, leads to a greater deterioration of the overall tree physiology than a single stress event [136,137]. Forest or agronomic tree management also appears to be related to the declines. It has been observed that Q. suber forests managed for a long period according to certification schemes (i.e., rational management of spontaneous vegetation, rotation of areas hosting cattle, delimitation of pasture areas) results in reduced COD [138]. An excess of herbicide distribution [106] causes nutrient imbalances in the soil of olive groves in Apulia that exhibit OQDS [107], whereas soil compaction, due to repeated tractor passes, predisposes the soil to a greater negative impact from excess water in KVDS-affected orchards [108].

The involvement of some aggressive phytopathogenic microorganisms is another notable similarity to highlight in all the declines described herein. Oomycetes for COD, SOD, and KVDS; bacteria for AOD; and X. f. subsp. pauca and Botryosphaeriaceae spp. for OQDS, once induced by a single stressor or a combination of abiotic stressors, can cause the final death of the plant, acting as a decisive contributing factor. All microbial species involved have their own ecology regarding their capability to display their aggressiveness toward host plant species. While the oomycetes affecting oaks and kiwifruit are typical inhabitants of soil and water [71,108,139], the bacteria involved in AOD inhabit diverse habitats: R. victoriana and G. quercinecans colonize various niches such as soil, leaves, and acorns; B. goodwinii and L. britannica are genuine inhabitants of acorns and most likely members of the seed endophytic community [140]. In contrast, the microbes involved in OQDS are typical colonizers of the aerial parts of the tree: leaf and twig for X. f. subsp. pauca, and twig and branch for the Botryosphaeriaceae [97,103]. One notable difference concerning oak declines is the apparent absence of Phytophthora species (i.e., P. cinnamomi, P. quercina, P. ramorum) involved in AOD, despite their occurrence in English forests and other areas of Europe [141,142]. One possible explanation for such an exclusion is that Phytophthora spp. exhibit relevant site specificity [142], and apart from the occurrence of water, they require specific edaphic conditions, such as higher carbon, nitrogen, and calcium soil content, and a pH above 3.5 to initiate the infection [24].

7. Perspectives

The decline of trees and perennial crops is an outstanding phenomenon observed in many areas of the world [1,7], and a clear relationship with global warming has been established [143]. Repeated droughts and waterlogging, two differing aspects of global warming [144], trigger many plant declines, including those concerning oaks, olives, and kiwifruit, which are herein described as relevant inciting stressors. A less obvious additional impact of such stressors is the significant disturbance to the soil microflora equilibria [145], leading to an overall negative effect on the microbes that live in closer contact with the plant (i.e., the rhizosphere), thus inciting specific plant dysbiosis [123,124]. To understand this intricate relationship between abiotic and biotic factors, it is necessary to add the notable role played by certain microorganisms, such as Oomycetes, Botryosphaeriaceae, X. f. subsp. pauca, and the AOD bacteria, which gain a decisive advantage from weakened host plants and can become quite aggressive.

Consequently, it is evident that tree decline is a complex phenomenon, and a comprehensive approach is required to dissect all the facets involved. For COD, SOD, AOD, and KVDS, a multifaceted approach to studying and analyzing both abiotic and biotic factors, including their interrelationships, has been widely applied. In contrast, for OQDS, most of the research has focused solely on the involvement of X. f. subsp. pauca [146]. The quarantine status of this bacterium should not preclude the investigation of the concurrent contributions from other factors, such as Botryosphaeriaceae species widely found in olive groves also affected by the bacterium, which have proven to be aggressive to olive trees [96,100,102], as well as the roles played by drought [99] and other stressors [147]. A better understanding of the various roles played by the concurrent presence of X. f. subsp. pauca and Neofusicoccum spp. in the same tree could assist in providing a more effective mitigation for olive decline [148]. Additionally, regarding oak and kiwifruit declines, it is now widely accepted that a greater understanding of altered host–microbial community relationships can lead to more tailored management of declines [114,116,118,149,150,151]. This approach is particularly valuable in a global scenario where the host plant and microbiota, including potential pathogenic species, are under the selective pressure of climate change, which induces extensive modifications in host plant physiology and the molecular components of the plant defense system, triggering consequent microbial adaptations [152,153]. Within this context, a more comprehensive approach is also required to investigate the direct influence that drought exerts on microbial communities to identify potential microorganisms capable of mitigating the damage caused by this stressor to the plant (i.e., plant-growth-promoting rhizobacteria) [154,155,156].

Resilience or symptom mitigation are other aspects closely related to the declines described herein. Resilience, defined as “the ability of a plant or an ecosystem to adapt to perturbations and to change or recover in such a way that maintains functions, structure, identity, and feedback” [157], is a goal to achieve for oak declines [158]. Forest certification for the rational management of space and land utilization by animals offers a reliable possibility to increase oak resilience [138]. Another possibility for recovering oaks affected by COD triggered by occasional droughts is thinning. The reduction of tree competition for soil water, indeed, improves long-term radial growth and allows us to reach the pre-drought growth rates [159]. The selection of oak varieties that demonstrate tolerance to drought can be useful in increasing overall tree resilience [160]. Resilience has also been observed in olive trees severely affected by OQDS [107]. Such trees, which host a high cell density of X. f. subsp. pauca and yield fruits, show an increase in certain hormones (i.e., jasmonic and salicylic acids) that could promote adaptation to the infection [161]. The mitigation of KVDS could be achieved by utilizing selected rootstocks that exhibit a high tolerance to soil hypoxia and enable the growth and production of the grafted cultivars [162,163,164,165,166]. It is noteworthy that Actinidia spp. assessed for rootstock selection shape the plant rhizosphere and endosphere pathobiome, with the most tolerant one displaying the capability to avoid Phytophthora root colonization [165].

The mitigation of symptoms in tree declines through the distribution of beneficial microorganisms or eco-friendly compounds is another possibility to pursue for maintaining tree vitality. Regarding COD, the good potential of native Trichoderma spp. isolated from healthy oak trees has been observed to protect the roots from P. cinnamomi colonization, thereby avoiding the risk of introducing alien microorganisms into the soil forest [167]. The endophytic mycoflora also presents potential to control certain fungi (i.e., Biscognauxia mediterranea and Diplodia corticola) involved in Q. suber decline [168]. X. f. subsp. pauca associated with OQDS can be effectively managed by applying a biocomplex to the tree crown, which reduces the cell density of the bacterium within the foliage and allows the tree to yield regularly [148,169,170]. A prompt site analysis that can reveal the initial occurrence of a forest or crop decline could enhance the possibilities of applying mitigation measures more quickly. Remote sensing and satellite imagery monitoring of a specific area can be very useful both in predicting risks for potential oak decline [171] and in revealing the occurrence of an impending decline [172]. Under a global scenario characterized by warmer temperatures and repeated drought events, the declines of perennial plant species will most likely accompany us in the future. Tree resilience in a warmer Earth should be retained as a primary goal to maintain both natural ecosystems and profitable crops [173,174].

8. Conclusions

The decline of perennial plant species is a complex phenomenon and should be framed and studied in a broad context that involves both abiotic and biotic causes, each acting as predisposing, inciting, and contributing factors. Such an approach is commonly applied to forest tree species; however, for agricultural crops, it is less common, and the traditional criterion of considering a single pathogen as the sole cause of tree dieback remains quite prevalent. The OQDS is a clear case where the importance of other factors, besides the one considered the sole cause (i.e., X. f. subsp. pauca), has not received much consideration.

The sudden OQDS outbreak in the olive groves of Salento, recorded around 15 years ago, seems perfectly framed within a local context characterized by a minimal application of agronomic techniques, repeated drought events, and prolonged heatwaves observed during the summer. The introduction of X. f. subsp. pauca from abroad, along with the contemporary occurrence of aggressive Botryospheriaceae, has contributed to this scenario, causing a severe decline in otherwise well-adapted local cultivars. Within this complex syndrome, the effective management of OQDS should consider a combination of different strategies, all aimed at reducing the impact of abiotic and biotic stressors on the crop (i.e., localized irrigation, maintenance of soil fertility, sustainable management of pathogenic microorganisms, vector control, and tolerant cultivars).

The importance of dissecting complex syndromes by analyzing either the abiotic or biotic factors involved is demonstrated by the achievements recently obtained for KVDS. A series of studies have shown how excess water in the soil strongly predisposes the plant to subsequent attacks by aggressive microorganisms. Rootstocks resistant to waterlogging appear to be an effective means to reduce the risk of KVDS in future kiwifruit orchards.

The attainment of oak resilience seems to be a more challenging goal due to the vast natural habitats these trees inhabit and the threats posed by global warming, particularly from drought and prolonged heatwaves. It should be noted that Quercus spp. shows some capacity to counteract the impact of drought by allocating a high proportion of primary production from photosynthesis to the root system. Additionally, oak can access deep groundwater by developing roots in deeper soil layers. Thinning and using non-harmful parasitoid insects to combat defoliating insects provide a possibility to mitigate some causes of decline. However, concerning the forest tree species, a policy aimed at reducing the Earth’s temperature increase in the mid-term and long term presents an opportunity to enhance the natural capacity for adaptation in such species.