Together with Septoria musiva, Discosporium populeum, also known as "Dothichiza", is one of the most widespread weakness parasites affecting poplars of section Aigeiros used for intensive cultivation. It is not improper to say that the measures adopted to combat its attacks, improving agronomic techniques, have increased the production through a rationalisation of some of the cultivation stages.
1.2.1.1. Symptoms and the damage caused - Necroses caused by D. populeum can impair the growth and often the survival of hosts during the whole vegetative season after the infections, though they usually begin in late autumn, or in late winter in the case of one-year saplings, when the same hosts are already in the resting stage. The target is one- and two-year-old nurseries or plantations up to three-years-old subjected to water stresses, often because they are located on too sandy soils prone to periodical water shortages, or due to the onset of a transplantation crisis or the concomitance of these two causes. At all events, a predisposing condition to the progression of infections is a dehydration of the cortical tissues that will subsequently be aggravated by the parasite.
The first visible symptom is the appearance of variously sized patches, pale maroon at first, then turning to brown, on parts of the bark near its various discontinuities: leaf scars, insertion points of buds and branches, separation rings between the annual shoots, abrasions, injuries or prunings. These patches, symptomatic of incipient necroses of large areas of the bark, soon extend, mainly along the axis of the infected organ, and their surface often sinks below the level of the surrounding healthy tissues due to progressive dehydration of the outermost layers. Exposure of the bark inner layers and of the adjacent wood circles shows that they are brown and marcescent, and sometimes damper than the non-infected areas.
At a later stage of the disease, some sections of the dead bark are lifted up by the internal pressure of the imperfect fruiting bodies that have formed in the meantime and soon split above them and expose them to atmospheric agents. These fruiting bodies, known as pycnidial conidiomata, are by now visible to the naked eye as coriaceous, blackish and globose corpuscles (Ø = 1-2 mm) with a small opening for dispersion of their conidia, erupting from the periderm of the stem or branch attacked, and often arranged in rows or in concentric circles around the penetration point of the parasite. If the weather is sufficiently humid, the conidia are released in a yellowish, mucilaginous substance and dispersed by the rain and the wind.
When the host starts to grow again, it can circumscribe the infection and react against it by forming callus tissues, if the water capacity of the soil has returned to optimum levels and if the portions of damaged tissue are not too many and/or too extensive, though complete healing is rather rare. In this stage, the disease takes on the appearance of a "canker" that in any event points to an active role on the part of the plant. On other occasions, especially if the state of hydro-physiological imbalance persists and the host does not have the resources needed to mount a reaction, the parasite kills other areas of the bark during the spring. These killed areas eventually occupy the entire circumference of the trunk and lead to the death of the part of the plant above. In the most serious cases, the annular extension of the necrosis is completed when the plant is still dormant and even the spring renewal of growth is lost.
Heavy attacks by D. populeum can both kill off much of a nursery's stock and also impair the further growth of the plants that remain and their subsequent planting out. Furthermore, plants that get over the critical stage of the infection run the risk of being broken off by the wind at their colonised areas. The quantitative damage is thus translated into loss of productivity or fewer poplar saplings available for sale. Nevertheless, adult plants with extensive infections have been observed in Italy in recent years, mostly in portions already showing the so-called "brown spots", reported on the "Luisa Avanzo" Euramerican clone, which is known to be sensitive to hydro-physiological imbalances. Since the brownings linked to the necroses in this case are peripheral when the wood is used, there is a loss of quality and hence a substantial decrease in the price of the ply-wood products.
1.2.1.2. The pathogen - Discosporium populeum (Sacc.) Sutton [= Chondroplea populea (Sacc.) Kleb. = Dothichiza populea Sacc. et Briard] is the name given to the anamorph of Cryptodiaporthe populea (Sacc.) Butin (fam. Valsaceae, ord. Diaporthales, phylum Ascomycota), whose fruiting bodies, once rarely found on dead organs, are observed with greater frequency today.
The parasite is found in most parts of the world. Its areale, whose extension has certainly been favoured by human activities, embraces Eurasia (India and China included), North Africa, North America and Argentina. There have been several epidemics, both in south-central Europe during poplar cultivation dawning at the start of the 20th century, and after the Second World War in most of Central Europe, particularly Bulgaria, Poland and the former Jugoslavia. Recrudescences in some poplar regions (e.g. in northern Italy) in the 1980s were attributable to the drier climate and the dissemination of new Euramerican clones, that were introduced on account of their resistance to Marssonina brunnea and their appreciable technological characteristics, but proved to be susceptible to D. populeum owing to their insufficient environmental adaptability.
The virulence of D. populeum seems confined essentially to Aigeiros section. It attacks both P. × euramericana, to an extent that varies from one clone to another, and P. nigra, whereas P. deltoides is more resistant (indirectly, due to its greater tolerance of water shortages) as are P. trichocarpa and the P. deltoides × P. trichocarpa and P. deltoides × P. maximowiczii hybrids.
1.2.1.3. Biology and relations with the host - Hydro-physiological imbalances, due to a substantial lack of rain and/or a too coarse texture of soil and/or the excessive competition for light and nutrients, frequent in nurseries or quick-turnover plantations, are predisposing to D. populeum infections of the host because of the more or less rapid dehydration of its cortical tissues. This is a necessary, though not sufficient prerequisite for the effective triggering of an attack: for this to happen, in fact, there must be penetration through a discontinuity of any kind in the bark, whether natural or artificial (referred to above when speaking about the location of the symptoms), that exposes the underlying vital tissues. Contamination usually takes place in spring; however, autumn is the best season for inoculation and infection, which proceeds during the following year. There are some reasons for this prevalence of autumn infections:
_ the ability of the plant to react is reduced, especially as the result of the long shortage of water during the summer;
_ the fungus can grow at low temperatures, and also takes advantage of the increase in relative humidity for the germination of conidia;
_ germination itself is boosted by the long autumn nights.
Several studies have shown that temperatures of about 10 °C, common in this period, do not hinder the fungus; in addition, they inhibit proliferation of the host's secondary meristems so that it cannot circumscribe the colonisation of its tissues, which increases in vigour as dehydration becomes more pronounced.
Conidiomata typical of the anamorph (whose appearance, described above, is a useful diagnostic factor) develop in the dead bark in late winter or early spring. The one-celled conidia, hyaline and ovoid (10-13 × 7-10 µm), form a sufficient vital mass of inoculum during most of the year, since they are released gradually on several occasions and maintain their viability for a long time (estimated at about five years in the laboratory). As already mentioned, however, the parasite transmission take place in spring, when transfer to new hosts is facilitated by the abundant equinoctial rains and the wind.
The teleomorph is provided by black, spheroid (Ø = 500-600 µm) and long-necked perithecial ascomata, later differentiated from the conidiomata, within which hyaline, two-celled, ovoid ascospores (16-23 × 6-9 µm) are formed. Its recent greater frequency has been seen as evidence of an insurgence and diffusion of biotypes endowed with greater virulence than the old populations, as would seem to be confirmed in isolates from various poplar-growing areas of south-central Europe. These «hypervirulent» strains, which can be regarded as one of the reasons for the recrudescence of attacks along with the resort to predisposed poplar clones and with prolonged dry periods, are also a cause of further concern for future developments of the disease, since it is well known that sexually-based genetic recombination is a potential source of phytopathological dynamism, with practical consequences readily imaginable.
1.2.1.4. Control strategies - It is necessary to exploit the resistance to D. populeum displayed by some North-American and Asiatic poplar species, as well as by intersectional hybrids. At the same time, as much as possible must be done to eliminate some of their basic adverse features, such as the fragility of the root apparatus and the vulnerability to the wind of P. deltoides, or the susceptibility to Melampsora medusae (a widespread rust agent discussed in § 1.4.1 of this compendium) of some genotypes of P. trichocarpa or P. deltoides × P. maximowiczii. This objective can be pursued through a rational genetic improvement, such as the crossing of resistant P. nigra genotypes, which yet exist, with the aforesaid species to obtain clones free from the defects typical of their parents. Account must none the less be taken of the fact that real resistance to bark necroses seems connected to a form of tolerance indirectly established by environmental adaptability of clones, rather than to the genetic stock.
While the use of plants with a constitutional resistance to the disease is an obvious step towards its prevention, equal attention should be directed to the application of rational cultivation practices ensuring that they are maintained in a good hydro-physiological state, especially in predisposing climatic or edaphic contexts. The greater managerial and financial effort associated with the constant and careful observation of these practices will probably be offset by the positive outcome of cultivation and hence of production in the nursery, while defective or negligent management, though less burdensome, could result in the loss of an entire crop. In this connection, it must be made clear that curative measures fit to restore a normal hydration of stricken plants are little more than palliative, especially in a nursery, since the reaction of saplings is uncertain and they will be hard to market in any event due to the marks left by the callus tissues. In a plantation, on the other hand, phytosanitary pruning of infected branches to reduce the inoculum centres may be advantageous, provided the saplings are not exposed to further water shortage stress.
A correct prevention during cultivation should be sought through the following measures:
_ establishment of nurseries on soils with good texture and structure to ensure sufficient water retention;
_ adequate spacing of the cuttings to reduce the effects of reciprocal competition;
_ irrigation, working of the soil, moderate use of fertilisers and of herbicides to prevent competition from weeds;
_ prevention of leaf diseases (especially rusts) that weaken the host and predispose it to infections by D. populeum;
_ uprooting of the saplings when it is certain that they are in the dormant stage;
_ their speedy and careful transport, preventing accidental bark damage;
_ their preventive immersion in water for 5-6 days, sufficient to re-establish optimum hydration;
_ gentle planting out at the right depth (2-3 m in sandy soils and 1-1.5 m in clayey or loamy soils) and encouragement of early resumption of growth, e.g. by an application of nitrate fertilisers.
Chemical control may be required in the nursery. For cuttings from clones that grow vigorously, often more vulnerable to water shortage stress and hence predisposed to attacks of the parasite, it is advisable to integrate the aforesaid cultural measures with some preventive fungicide treatments, at first when a nursery is established and then twice a year between May and June. Solutions containing hexaconazole (3 mL/hL a.i.), carbendazim (25 g/hL a.i.) or chlorthalonyl (120 mL/hL a.i.) have proved effective for this purpose.
Biological control has not yet shown signs of producing satisfactory results.
Like the better known Discosporium populeum, the Cytosporae are virtually cosmopolitan parasites and appear in stands subjected to some form or stress or poor agronomic management, often in the train of an attack by the former. Correct application of the culture measures against the same D. populeum (see § 1.2.1), however, should also serve to extinguish the possibility of their appearance.
1.2.2.1. Symptoms and the damage caused - Infection begins in the late autumn or in winter, when the host is dormant. It strikes nurseries already stressed for other reasons, saplings prior to being planted out and recently established plantations. Adult trees too can be attacked by Cytosporae, if they are in a state of advanced decline, and in this case the fungus behaves as a distinctly secondary parasite.
The main species in terms of diffusion and severity of attacks is C. chrysosperma. It causes a slight depression and brown to blackish staining of the bark infected areas and of the underlying tissues, both symptomatic of an extending necrosis against which opposition on the part of the host is weak until the vegetative season begins. This is particularly true with regard to the more delicate stems and branches, which may succumb to withering if ringed by this necrosis, whereas the sturdier ones are often in time to build up a resistance to further invasion. The disease than appears as small brown depressions bounded by distinct calluses. On P. tremuloides and P.alba the fungus turns the bark orange beside the infection sites.
At the end of the winter, pycnidial conidiomata differentiated by the parasite in the dead tissues gradually push up the outer layers of the bark. These fruiting bodies are of diagnostic value, since they are clearly smaller (Ø = 0.5-1 mm) even to the naked eye than those of Discosporium populeum and more randomly arranged. They remain within the cortical tissues of the host and only their ends, each with a minute orifice called an ostiole, are exposed to the environment, where they release masses of conidia suspended in linear or spiral mucilaginous cirri, orange-yellow in the case of C. chrysosperma, that are dissolved and dispersed by the rain.
In the advanced stage of the disease, the dead bark tissues that have not formed a callus peel away to reveal the underlying wood, marked with red-brown bands that eventually turn black.
Attacks by C. nivea and C. ambiens are usually more occult. Since there is no browning of the bark infected areas as in the case of C. chrysosperma, signs of infection are only visible when the conidiomata partly emerge on the non-darkened surface. Another diagnostic character is provided by the different colours of the mucilaginous cirri released by the three species (Table 1).
Except in some restricted geographic regions, the incidence of the Cytosporae is less than that of D. populeum. The kind of damage they cause is exactly the same, however, and reference can be made to what was written with regard to the latter (see § 1.2.1). Secondary infections by C. chrysosperma are often responsible for a further loss of production when it attacks stems and branches already damaged by D. populeum or Septoria musiva, another significant agent of bark necrosis.
1.2.2.2. The pathogens - The form-genus Cytospora Ehrenb. embraces the anamorphs of many Valsa Fr. species (fam. Valsaceae, ord. Diaporthales, phylum Ascomycota), including facultative parasites very widely found on several broad-leaved trees and characterised by a polyphagy that may be more or less marked according to the species.
C. chrysosperma (Pers.: Fr.) Fr. (teleomorph: V. sordida Nitschke) only infects Salicaceae. It is of little consequence in natural stands, but of primary significance in intensive poplar growing, where its opportunism is favoured by the application of slack cultivation criteria. Found almost everywhere in the world, its highest incidence is in central and southern Italy, eastern Europe, the Near East, northern India (mainly in plantations) and in west-central U.S.A. (especially in Colorado, where it also attacks natural formations of P. tremuloides). Its poplar hosts belong to the Aigeiros, Tacamahaca and Leuce sections (mainly on the just cited P. tremuloides), though its virulence sometimes varies from one isolate to another.
The polyphagous C. ambiens Sacc. (teleomorph: V. ambiens Sacc.) and C. nivea (Hoffm.) Sacc. [teleomorph: Leucostoma niveum (Hoffm.: Fr.) Höhn. (= V. nivea Fr.)] are more sporadic on poplars, though the latter is not uncommonly observed in southern Africa.
As already mentioned, these three species give rise to distinct symptoms on poplars and differ in some morphological and/or morphometric features of their conidia and spores (Table 1); their conidiomata, however, are always plurilocular (i.e. their interior is divided into some compartments sharing a single orifice), and their conidia are always one-celled, hyaline, cylindrical and curved.
1.2.2.3. Biology and relations with the host - The establishment of Cytosporae on the host, their fructification times and patterns, the dissemination of their conidia and the progression of the cankers they cause are very similar to those of Discosporium populeum. Unlike the latter, however, the teleomorph rarely appears on infected tissues and is of virtually no phytopathological consequence. C. chrysosperma has also been shown to start latent infections in buds, that then extend to the bark in case the plant becomes weak.
C. chrysosperma is generally less pathogenic than D. populeum, though it is a more powerful saprophyte that not uncommonly attacks nearly dead adult trees and appears on saplings already invaded by other bark parasites. It is in any event a very plastic organism, capable of vegetating - as shown by its virtual ubiquity - in a very wide range of climates, though it tends to focus on areas subject to drought at least for part of the year, and its effect increases the more a plant is distressed.
Experiments revealed a substantial analogy between the physiological consequences of water shortage and defoliation on the host, consisting in a decrease of carbohydrates in the cortical tissues which, through complex biochemical reactions, causes an impairment of its ability to prevent the establishment of Cytosporae. Defence mechanisms such as the production of periderm and lignification of the cells near the infection sites are inhibited; direct stimulation of the growth of C. chrysosperma by tissue dehydration, however, seems less likely.
Table 1 - Different morphological and morphometric characters of the Cytosporae reported on poplars (from Lanier et al., 1976; modified).
Anamorph: |
C. chrysosperma (Pers.: Fr.) Fr. |
C. ambiens Sacc. |
C. nivea (Hoffm.) Sacc. |
Teleomorph: |
Valsa sordida Nitschke |
V. ambiens Sacc. |
Leucostoma niveum (Hoffm.: Fr.) Höhn. (= V. nivea Fr.) |
Symptoms: |
bark browning emerging conidiomata |
emerging conidiomata |
emerging conidiomata |
Colour of cirri: |
orange-yellow |
yellowish-white |
red |
Conidium size: |
3-5 × 0.5-2 µm |
5-7 × 1 µm |
6-7 × 1.5-2 µm |
Ascospore size: |
12 × 1.5-2 µm |
16-18 × 3-4 µm 20-26 × 5-6 µm |
12-14 × 3 µm |
1.2.2.4. Control strategies - A specific genetic selection of resistant clones is unfeasible against C. ambiens and C. nivea and also seems poorly practicable against C. chrysosperma, since the host's genetic stock is of marginal importance for the growth of the disease by comparison with its physiological state. Nevertheless, it might exert an indirect influence through the environmental adaptability of the various clones, insofar as more constitutionally balanced clones with a harmonious development of the epigeous parts and of the root apparatus, and not excessively directed to productivity alone, will be preferably employed, since they will be less likely to fall into the states of distress that open the way to the disease.
Due to their many affinities, what has been said on the subject of cultivating and chemical control with regard to D. populeum is equally applicable to the Cytosporae. As already mentioned, measures taken to prevent attacks of the former should shield from the latter too.
Hypoxylon mammatum is an ascomycete responsible for the most serious disease to which P. tremuloides is exposed. This tree is widely distributed in North America as a component of either pure or mixed forests and is highly regarded as the source of clones suitable for the intensive production of fibre wood in temperate and cold climates. Heavy attacks by H. mammatum have been the cause of heavy economic and ecological repercussions for decades, especially in the U.S.A. on account of the importance of its preferred host, while in recent years there have been growing reports of attacks on other species, especially members of the Leuce section, in several parts of Europe.
1.2.3.1. Symptoms - Attacks by H. mammatum occur in natural formations, both pure and mixed, of P. tremuloides in the U.S.A. and - to a lesser extent - of P. tremula in Europe, as well as in tall timber stands, especially in those substantially thinned out where the plants keep their lateral branches for a longer period. Infected trees are sometimes more frequent on the edges of a wood, but usually their distribution in the interior is nearly casual, which means that their closeness to healthy trees does not always increase the probability that these will be infected. Both young and adult trees are attacked, the former on their main stem, the latter mainly on their branches, through which the fungus then may reach the trunk. In fact, cankers are often observed around dead branches, pruning cuts and the holes made by xylophagous insects.
A typical set of symptoms appears on P. tremuloides and P. tremula, with an often deadly outcome. A brown to blackish fluid exudes from the infected portions of the bark, which at first are orange-yellow and slightly sunken compared to the surrounding healthy bark. These areas then crack along necrotised rectangular laminae that eventually fall off and expose the inner cortical tissues and the first woody circles, which are blackened and crumbling. The necrosis moves much more quickly along the axis of the stricken organ, whereas its transverse extension is sometimes checked by the formation of a reaction callus on the part of the host. Cases of regression, however, are extremely rare6. Old cankers are thus narrow and even more than one metre in length; their centre consists of a rough, blackish surface, surrounded by a cracked strip in the process of peeling off, whereas the borders of further expansion are yellowish. Removal of the bark along these ones reveals a white mycelium arranged like a fan of on the cambium.
From 5 to 14 months after the infection, in a period which runs from spring to the height of summer, a stromatic mass appears under the periderm of the cracked peripheral strip. This supports the fructifications of the anamorph (ascribable to Geniculosporium Chest. et Green) in the form of a dusty, bristle-like grey layer composed of several synnematal conidiomata. It is the growing pressure of this layer on the inner surface of the periderm that results in its peeling away from the innermost tissues, so that the conidia can be dispersed. While the fungus attacks new portions of the trunk, the anamorph fructifications that thus find themselves in a central position disappear little by little. The teleomorph, consisting of perithecial ascomata partly immersed in carbonaceous sexual stromata, appears three years after the infection in the blackened, marcescent areas mentioned earlier.
1.2.3.2. Incidence and the damage caused - Studies of P. tremuloides stands have shown that, despite the notable incidence of the disease on plants in all diameter classes, younger trees display a proportionally higher mortality rate because the cankers form on their main trunk. Instead, in adult trees the branches are primarily affected, and their foliage is thus weakened due to impairment of the conducting tissues, but they are rarely killed by annular necrosis at their base. This last phenomenon is more likely on the upper zone of the trunk and result in withering of the portions of foliage above it; the plant can, however, survive by activating, as a dominant shoot, a branch or a bud below the necrosis. The marked mortality of the younger trees, on the other hand, especially those less than 9 cm in diameter at breast height, is caused by direct infection of the trunk, whose entire circumference may become necrotic in the space of a few years. Both young and adult plants are also likely to be broken by the wind at the canker sites, since their underlying wood is also degraded by the parasite.
H. mammatum is thus responsible for both quantitative and qualitative damage: economic losses of the order of millions of dollars a year in the time of utilisation are caused in the U.S.A. The data concerning its incidence on P. tremula in Europe are fragmentary. Nevertheless, the frequency of infections was valued on high levels in stands of the southern Alps and the southern Jura where, according to Pinon (1986), up to 10% of trees display signs of disease.
1.2.3.3. The pathogen: taxonomy and geographical diffusion - Hypoxylon mammatum (Wahl.: Fr.) P. Karst., long cited as H. mammatum (Wahl.) J.H. Miller [= H. pruinatum (Klotz.) Cke.], is a member of the fam. Xylariaceae (ord. Xylariales, phylum Ascomycota). A recent suggestion is that it should be renamed Entoleuca mammata (Wahl.: Fr.) J.D. Rogers et Y.-M. Ju, on account of certain morphological characters regarded as excluding it from the genus Hypoxylon Bull. sensu stricto as this is understood today.
In addition to various poplar species, it has been reported on willow, birch, alder, hornbeam, beech, elm, sorb, pear-tree and spruce. Crossed inoculations of isolates have revealed a certain degree of host specificity, though not enough to justify the creation of separate species, since there are no significant morphological differences with regard to ascomata and ascospores. The pathogenic potential of H. mammatum, however, is only realised to the full on poplars, especially on some members of the Leuce section, namely P. tremula, P. adenopoda (Chinese aspen), P. grandidentata and above all P.tremuloides, and also - to a lesser extent - on P. alba and P. × canescens. Among the Tacamahaca, cases of infection have been reported on P. trichocarpa, with a more or less positive outcome depending on the clone concerned, and on P. balsamifera, though rarely. Hybrid clones can also be attacked if one of their parent lines is susceptible.
The areale of the pathogen has been defined in general terms, though some uncertainties remain. It covers the whole of North America, but the incidence of the disease is only heavy in the Great Lakes Region and the Prairies of the North-West, whereas it is secondary in the central section of the Rocky Mountains and even negligible in their northern section and in Alaska, where yet P. tremuloides is abundant and the fungus is regularly reported, even as an asymptomatic endophyte. Its distribution in Europe is irregular; the specific literature contains reports from much of France (with a high incidence in the southern sectors of the Alps and the Jura, characterised by more irregular precipitations), Andorra, Great Britain, the Swiss Jura, some upland and highland areas in Italy (western Alps and Tuscany), Sweden, the Czech and Slovak republics and some parts of Russia. Although all these reports are rather recent, it is believed that H. mammatum has long been present in Europe and may indeed be autochthonous.
1.2.3.4. Biology and relations with the host - Many aspects concerning the inoculation of H. mammatum in nature, the infection, the role of the environmental variables and the sources of host resistance are still not entirely clear. The fungus can be said to be a recurrent endophyte of several broad-leaved trees. Its pathogenic potential is only triggered by the concomitance of some circumstances, some of which are under specific genetic control. This would explain why the induction of the disease is restricted to some poplar species, and indicates that the real geographic distribution of the fungus is very much wider than that documented by the canker appearance.
The relative importance of conidia, myceliar fragments and ascospores in the diffusion of the disease was very doubtful until a few years ago, but it is now considered that ascospores are the most important. Brown and ellipsoid (20-34 × 9-14 µm), one-celled, they are produced inside globose perithecial ascomata (Ø = 1.5 mm), covered by a greyish efflorescence in the young stage, assembled in groups of 4 to 30 in black and coriaceous stromata. These ascomata contain paraphyses (specialised hyphae that facilitate dissemination) and cylindrical asci (140-200 × 12-16 µm), which pass through the ostiole one at a time and release the ascospores one by one whenever the stroma is wet and the temperature near the bark is above freezing, usually at the end of autumn or the beginning of spring. If the humidity is sufficient, dissemination proceeds according to a 12-hour cycle, taking advantage of strong and weak currents of air for the horizontal and vertical dispersion of ascospores respectively.
The disease development is not dependent on weakness of the host; in any case, the susceptibility of this one to infections is determined by its genetic stock (at least in terms of sensitivity to phytotoxins produced by the parasite and of reaction to colonisation), by environmental and/or cultivation conditions, by the presence of animals responsible for the creation of potential infection sites. It seems certain that penetration, at least of the main trunk, requires a breach, however tiny, in the bark so that the cambium or the xylem is exposed. In fact, the germination of ascospores is prevented by both the green layer and the secondary phloem. The outer woody tissues, however, are colonised first, whereas the cambium and the cortical layers are only killed in a second stage. This prevention is due to the prior production by the host of fungistatic compounds (cathecol, salicin, salicortin), and also - though there is no consensus on this point - by an ex novo synthesis, stimulated by the presence of the fungus, of low concentrations of other more specific inhibiting compounds (phytoalexins). Even mild water stress, not necessarily demonstrated by the plant with manifest decline, assists infection in two ways, namely by depressing the production of the aforesaid inhibiting substances and by increasing the concentration of some aminoacids (proline, alanine, glutamine) that stimulate myceliar growth. It is also been demonstrated that fertilisers with an abundance of nitrogen compared with phosphorus and potassium encourage the onset of cankers, since plants grow with more succulent tissues, rich in proteins required by the parasite. In the Great Lakes Region, where the incidence of the disease is highest, a very high percentage of cankers are associated with wounds caused by insects, such as the oviposition scars made by Rhynchota [e.g. Magicicada septendecim (L.)] and especially the galls formed after oviposition by wood borers (above all Saperda inornata Say), in whose central tissues ascospores are not exposed to the action of the fungistatic compounds. Penetration may be also assisted by downy woodpeckers (Picoides pubescens L.), which feed on these insects and cause wounds that extend down to the xylem. By contrast, other canker agents frequent in the Rocky Mountains and endophyte fungi in the bark are thought to compete with H. mammatum and thus oppose its infections.
Much uncertainty persists concerning the real pathogenic importance of the phytotoxins (including that with the highest concentration, hymatoxin A), produced in varying amounts by individual fungus isolates. No correlation has been demonstrated between the sensitivity of P. tremuloides clones to these toxins and their susceptibility to the onset of cankers, suggesting that these metabolites are secondary determinants, in other words that they contribute to the virulence but are not needed for the establishment of the disease.
Lastly, some ambiguity is attached to the function of the one-celled, hyaline and fusiform (2-3 × 5.5-6.7 µm) conidia, which are omnipresent in nature where there are cankers, but have a very limited ability to give rise to colonies. It has been suggested, though not yet demonstrated, that they are involved as spermatia in the sexuality of the fungus.
1.2.3.5. Control strategies - One essential preventive measure is the avoidance of exchanges of wood infected by H. mammatum, even between countries where the fungus is already present, since this could lead to the reciprocal introduction of strains that might prove more virulent in contexts differing from those of their origin with regard to the environment and the genetic stock of their host, as well as the latter's associated mycoflora and its interactions with the same pathogen.
Exclusive control must obviously be accompanied by the search for the most resistant genotypes. This can be greatly accelerated by inoculation tests on saplings, which have proved reliable and in the space of a few days can indicate the rate of lignin deposition in the cell walls and the ability to form callus tissue in response to the infection, both of which are characteristics associated with a plant's susceptibility in the field. Genetic selection, indeed, is the indispensable prelude to the extended use of Leuce species for the intensive production of fibre wood in forest stations or on hydromorphous soils.
Chemical control seems out of the question in situations where attacks by H. mammatum are recurrent, and sanitation measures, designed to wipe out the disease from a stricken station, have proved to be fruitless. P. tremuloides stands with more than 25% of their trees infected must be felled as soon as they reach an appropriate mean diameter, and then replaced with other species or at least with genotypes whose resistance has been established.
The incidence of the disease can be substantially limited through a proper silvicultural management, which must provide for few, slight thinnings, found favourable to infections, and the attainment of fully stocked uniform stands.
Other pathogens infect both the trunk and branches, and sometimes result in combined attacks by different entities on the same poplar districts.
These pathogens are not presented here as a subordinate group because they are of secondary phytopathological importance, but because they occur in particular contexts: some are wound or secondary parasites that are present in a latent state in most poplar cultivations and only launch an attack in certain growing and/or environmental conditions; others have a currently limited areale, but are strongly pathogenic and responsible for considerable damage in the involved regions.
1.2.4.1. Cankers caused by Phomopsis spp. - Necroses or cankers caused by fungi belonging to the form-genus Phomopsis (Sacc.) Bubák were reported in all areas where poplars are intensively cultivated, more frequently in the warm-temperate and sub-tropical zones, including those where poplar growing have been recently introduced, such as southern Africa or India. Common features of these reports, whether remote (in Italy and Germany since the beginning of the century) or contemporary, are the rarity or absence of the teleomorphs - which are ascribed to Diaporthe Nitschke (fam. Valsaceae, ord. Diaporthales, phylum Ascomycota), with black perithecial ascomata and two-celled hyaline ascospores - and an occasional recurrence of these parasites in nurseries in precarious conditions or subject to water stresses. The pathogenic activity of individual species seem fluctuating in certain areas: long periods in which the parasite is apparently absent alternate with others marked by a considerable incidence, sometimes during or after a dry period.
As weakness parasites, the poplar Phomopsides attack more or less debilitated saplings with at least partially dehydrated cortical tissues, via small breaches in the bark itself or leaf scars. The cultivation conditions in which they act - almost solely in the nursery - are similar to those described for the more pathogenic Discosporium populeum, from which they also differ in the limitation of their infections to very young shoots or to the less lignified apical portions of the trunk and the branches. In temperate climates, the hosts are more susceptible during their winter rest, due to their reduced ability to oppose infections and to the lower tissue hydration, often typical of this phase.
The symptoms of attacks by Phomopsis spp. are much the same as those induced by D. populeum; diagnosis must thus be based on examination of some of the macroscopic and microscopic characters of the anamorph fruiting bodies. The pycnidial conidiomata of Phomopsis spp. (with the exception of P. macrospora) are smaller than those of D. populeum and conidia are emitted in mucilaginous cirri that are paler than those of Cytospora chrysosperma, which is also widely diffused in warm-temperate areas and causes similar symptoms. A peculiar feature is the production of two differently shaped one-celled, hyaline conidia: those of shape A are from ovoid to fusiform, those of shape B are filamentous, straight or curved. The individual species, especially those encountered in Europe, are mainly distinguished in the light of their morphometric characters (Table 2); uncertainties persist, however, and the employment of modern biomolecular diagnostic techniques would be advisable. The following species were found on poplars:
- P. putator (Sacc.) v. Höhn., reported at the start of the twentieth century in Germany and more recently in Italy and Argentina, on Aigeiros hybrids;
- P. populina Vogl., reported in the past in Italy on Aigeiros clones of the so-called "Canadian" type;
- P. pallida (Fck.) Sacc. et D. Sacc., reported in Portugal and Italy from the 1940s to the 196Os as mainly virulent on Populus deltoides, but also on Populus alba;
- P. tirrenica Moriondo, reported on Euramerican clones (including "I-214") in Italy since the early 1960s;
- P. macrospora Kobayashi et Chiba, reported in Japan and present with more continuity in the U.S.A. along a belt running from Minnesota to Mississippi, both in nurseries and plantations up to three years of age, on Populus deltoides, Populus × euramericana (including clone "Robusta"), Populus nigra and Populus maximowiczii.
An effective control of these parasites, too, must be primarily based on the application of careful cultural practices, designed to prevent saplings from damage and dehydration. Pruning residues are readily colonised by Phomopsides and their removal is an important step towards the extinction of sources of inoculum.
Table 2 - Morphometric characters of Phomopsis spp. reported on poplars (measures in µm).
|
Species |
Conidiomata |
Conidiophores |
Conidia | |
A |
B | |||
P. putator (Sacc.) v. Höhn. |
250 × 500 |
10-15 × 1.5-2 |
8-11 × 2.5-3.5 |
25-35 × 1-1.5 |
P. populina Vogl. |
200-400 × 200-250 |
16-24 × 3 |
8 × 3-3.5 |
24-40 × 1-1.5 |
P. pallida (Fck.) Sacc. et D. Sacc. |
150-400 × 120-160 |
15-20 × 3 |
5.5-9 × 1.8-2.2 |
14-24 × 0.4-0.7 |
P. tirrenica Moriondo |
400-1000 × 250-500 |
10-20 × 1-2 |
14-20 × 2-4 |
absent |
P. macrospora Kobayashi et Chiba |
3000-5000 |
7.5-9 × ? |
14-19 × 3-3.7 |
13-17 × 1.5 |
1.2.4.2. Necroses and cankers caused by Fusarium spp. - Various species of the form-genus Fusarium Link - whose teleomorphs are referable to Gibberella Sacc. (fam. Hypocreaceae, ord. Hypocreales, phylum Ascomycota), rarely seen on infected hosts - cause characteristic cankers, sometimes called fusarioses, on poplars from various sections. They are all markedly polyphagous, both on poplars and on other broad-leaved trees and herbaceous plants in the temperate zones. Geographical distinctions with regard to Populus thus are aleatory.
F. avenaceum (Fr.) Sacc. is perhaps the most important species at present. First reported in the 1950s on Euramerican clones in France, it has since spread to very different parts of Europe, ranging from central and eastern areas with a continental climate to sub-mediterranean areas and recently to Portugal with its oceanic climate. F. solani (Martius) Sacc. emend. Snyder et Hansen, found on Aigeiros and Tacamahaca poplars and intersectional hybrids, originally seemed to be confined to North America, but then has been reported in Poland too. Sporadic and of limited importance are F. lateritium Nees, observed in some parts of France and in the U.S.A. on P. trichocarpa, and F. sporotrichioides Sherbakoff, reported in eastern Europe and in central Italy on P. × euramericana.
The genetic component is of little consequence in fusarioses. The predisposing factor is distress of the host due to a shortage of water or poor growing conditions, such as the excessive crowding typical of many nurseries. Nevertheless, the inoculation seems to require discontinuities or points of greater vulnerability in the bark, preferably at the boundary between two vegetation stages or at shear planes. Some workers have suggested that latent infection of tissues surrounding the buds can also take place. Laboratory experiments have shown that the fungus is thermophilous to a certain extent, and this explains why its host is most susceptible in spring, when vegetative resumption is at its height, by contrast with the attacks of other bark parasites.
The incidence of the Fusaria is not comparable with that of Discosporium populeum in absolute terms. They are, in fact, almost solely a cause of concern in nurseries, especially on first-year and sometimes second-year saplings, where their initial appearance on a few plants may be quickly followed by involvement of the entire stand. Attacks on 10- to 15-year-old adult trees by F. avenaceum has occasionally been reported; in any case not more than 10% of the plantation is affected, while the symptoms are not immediately visible and mostly take the form of disorganisation of the cortical tissues in a preferential belt of the trunk 4 m to 8 m in height from the ground.
In the nursery, F. avenaceum is responsible for a characteristic set of symptoms. Swellings of the infected areas, often at the transition ring between one vegetation stage and the next, are soon followed by numerous close together longitudinal fissures, known to growers as "cat scratches", that advance in step with the necrosis of tissues and to the point where the bark almost begins to fray. During the late spring and summer, these lacerated areas take on a typical reddish to purple colour, typical of F. avenaceum, due to the presence of its mycelium. Cushion-shaped necroses with a different appearance sometimes form around the buds, on which fruiting bodies of the anamorph (sporodochial conidiomata) differentiate in conditions of high atmospheric humidity. The elongated, sickle-shaped conidia (14-40 × 3-5 µm), usually divided by 3-4 septa, are released in mucilaginous masses that are subsequently diluted by the rain. During the vegetative season, the stricken saplings almost always succeed in halting the further spreading of the necroses through the formation of evident callus tissues, showing thus the cankerous stage of the disease. Although the survival is assured, their marketability is greatly impaired, since these callus zones, within which the parasite has in any event disorganised the initial woody cell layers, are preferential sites for breakage even on the part of moderate winds, as well as being vulnerable to attacks by other bark parasites also active during a plantation's early years, such as D. populeum and Cytospora chrysosperma.
The symptoms of an attack by F. sporotrichioides are very similar, whereas F. solani causes the appearance of brownish necroses that are accentuated by the concomitant action of other Fusaria and of Geotrichum Link species. In north-eastern Europe it has been observed that pathogenic strains of F. solani can also be responsible for the degeneration of hyphae and conidia of Ceratocystis fimbriata, another poplar pathogen that causes what is known as "black canker" or "target canker", and that both fungi are sometimes isolated from lesions of this type.
As can be said with regard to the other bark parasites, the control of Fusaria first of all is founded on good nursery practices. Cuttings must be protected from physiological stresses as far as possible, especially with respect to the high reciprocal competition imposed by an excessive density, and care must be taken to avoid damaging their bark. The genetic selection of possible resistant clones is not for the present a viable solution, since the degree of susceptibility of existing clones is not yet well known and the relative weight of the genetic component compared with the environment is still uncertain. Chemical control is about the same as for D. populeum.
1.2.4.3. Sooty-bark canker caused by Encoelia pruinosa - Encoelia pruinosa (Ell. et Ev.) Torkelsen et Eckblad [= Phibalis pruinosa (Ell. et Ev.) Kohn et Korf = Cenangium singulare (Rehm) Davidson et Cash] is a discomycete (fam. Leotiaceae, ord. Leotiales, phylum Ascomycota) responsible for a serious canker on P. tremuloides and, to a very secondary extent, on P. balsamifera. The disease involves a very wide geographic belt, similar to the areale of P. tremuloides natural forests, running from Alaska through western Canada and along the Rocky Mountains, with extensions to some of the Mid-west States, down to northern Mexico. Besides, the pathogen was observed in Norway.
E. pruinosa is a wound parasite and thus easily able to attack P. tremuloides, whose soft bark is readily damaged by climatic factors, animals and humans. Recent surveys in natural formations have shown that its incidence on all live plants is low (of the order of 1%), but much higher when only mature and overmature trees (aged 100 to 120 years) are considered, contrary to what is observed with Cryptosphaeria lignyota (Fr.: Fr.) Auersw., another bark canker agent that attacks this host (see § 1.2.4.4).
The symptoms are rather characteristic: colonisation is revealed by an elliptical area depressed with respect to the still healthy surrounding bark, arranged around the infection site, in rapid extension throughout the year without the host being able to form an effective callus of reaction. The dead tissues become more striking after 2-3 years, when the pale outer layer of the bark begins to peel off and expose the thicker inner layer, which is blackish and remains tightly attached to the trunk even for a long time after the plant is dead. When touched, its surface crumbles and leaves a sooty deposit on the fingers, hence the common name of the disease. The fungus seems to cement this layer to the wood below, to which it confers a design composed of dark spots on a paler background, visible when the same layer finally falls off in long fibrous strips.
By contrast with most bark parasites, only the teleomorph of E. pruinosa has so far been found in the field. This consists of externally pale grey apothecial ascomata in the shape of irregular cups (Ø = 3 mm), produced in large numbers on the old blackened bark or under the thin whitish outer layer. The ascospores are primarily disseminated by the wind all through the year, whenever the temperature and humidity are right. In the laboratory a conidial form has been obtained, variable according to the medium and growth conditions, and comparable at times with Acremonium Link and at times with Myrioconium Syd., whose importance in nature, if any, remains to be determined.
Sooty canker is a serious disease on P. tremuloides, especially on large trees, mainly because its appearance does not leave any way of escape for those that are stricken and their chances of mounting a successful reaction are very small. Statistical analysis has shown that the mean expansion rate of a typical canker lesion around the circumference of the trunk is about 16 cm/yr, which is enough to kill a tree in a few years. It is estimated that more than half of the deaths in natural and nature-like forests of this poplar species are directly caused by E. pruinosa.
1.2.4.4. Snake canker and wood decay caused by Cryptosphaeria lignyota - Like Encoelia pruinosa (see § 1.2.4.3), Cryptosphaeria lignyota (Fr.: Fr.) Auersw. [= C. populina (Pers.) Sacc.] (fam. Diatrypaceae, ord. Diatrypales, phylum Ascomycota) is a pathogen especially present on P. tremuloides, within an area of activity that runs from Alaska and Yukon Territories along the western U.S.A. down to Arizona and New Mexico. It has also been reported in some central and eastern States, e.g. Minnesota, Michigan and Pennsylvania, where it may attack other poplar species (P. balsamifera, P. trichocarpa, P. deltoides), as well as willow (Salix purpurea L.). At present, its incidence is confined to North America; further epidemiological developments, however, may be foreshadowed considering that more than a century ago the fungus was found in Europe on P. tremula, P. alba and P. nigra.
C. lignyota is a canker agent that mainly infects young P. tremuloides trees in natural formations, with a diameter at breast height of not more than 30 cm, and more frequently the younger they are. It can also infect buds and branches and then pass to the main trunk to induce a typical canker syndrome. More mature trees are not affected by the disease, possibly because the fungus is in some way limited in both its penetration of very thick barks and the expression of symptoms on the same. The pathogen is important not only as a bark parasite, but also on account of its ability to reach the central cylinder of even mature trees and behave like a wood decay agent.
The penetration stage requires a breach in the bark or, otherwise, the infection may also spread from previously stricken organs of the plant. The cankers are usually long and narrow, sometimes coiled around and along the trunk like a snake due to the marked difference between their longitudinal and their lateral progression, surrounded by areas of ochreish or orange bark, symptomatic of the advancing colonisation. Callus formation does not become apparent for at least two years after infection and is often unable to prevent its further extension. Bark tissues dead for at least a year, tightly attached to the sapwood, become black and fibrous, like those found in E. pruinosa cankers, from which they are distinguished by the presence of scattered elliptical pale spots (Ø = 0.5-2 mm). The perithecial ascomata typical of the teleomorph develop in a very compact, narrow myceliar matrix (pseudostroma) that works its way under the periderm of this dead bark and may be up to 30 cm long. In some instances, acervular conidiomata of the anamorph differentiate on the edge of the cankers; these are pale orange and produce one-celled, filiform and curved conidia assigned to Libertella Desm.
The anamorph is often isolated as a decay agent from both the heartwood and the sapwood, where it induces various colourings: grey in the sapwood under the cankers of thinner trunks, from brown to yellow and on to pink with mottles in more mature trees.
The parasite can kill young trees within a year from infection and contributes to the natural thinning of P. tremuloides formations. It would seem that often the host's death is not due to annular extension of the canker, but to a massive invasion of the sapwood that prevents it from transporting water and nutrients. Owing to its marked preference for shoots and young trees, the wood decay it causes and its proven ability to establish itself on a variety of poplar species, C. lignyota is also a potential threat to intensive poplar growing, and strict vigilance is essential to avoid its introduction.
1.2.4.5. Black or target canker caused by Ceratocystis fimbriata - Several species of Ceratocystis Ell. et Halst. (ord. Microascales7, phylum Ascomycota) were reported in association with cankers on poplars.
The only one of remarkable phytopathological importance is C. fimbriata Ell. et Halst. [= Endoconidiophora fimbriata (Ell. et Halst.) Davids.], a parasite very widely distributed in temperate and tropical environments and on the whole very polyphagous, since it is able to attack roots, stems or fruits of both herbaceous plants (sweet potato, cacao, coffee) and trees (various species of Prunus L., rubber trees and above all planes, on which, with the f. sp. platani Walter, it causes a pernicious tracheomycosis known as "black stain"). On poplars, too, its range of action is being gradually extended. Up to twenty years ago, its manifestations were confined to Alaska and the Rocky Mountains, where it is one of the main agents of cankers in natural P. tremuloides stands - rarely fatal on the other hand -, and more sporadically to a few of the north-eastern U.S.A. and Quebec. Attacks of a certain seriousness have since been reported on adult plantations in Poland, especially on some Tacamahaca, Tacamahaca × Aigeiros and Aigeiros × Tacamahaca hybrid clones, and more recently, though with a secondary incidence, on P. deltoides in India.
C. fimbriata penetrates into the trunk through the insertion points of small branches, as well as through wounds, frequently opened in the tender thin bark of P. tremuloides. In the forest, it mainly attacks trees with a diameter of about 40 cm, but not the older ones. The symptoms are similar on P. tremuloides and on the hybrids mentioned above: the first sign is a slight depression in the bark, which gradually turns brown starting from the infection point and, in the following spring, is circumscribed by a vigorous callus. During the subsequent vegetative repose, this too is colonised and killed by the parasite, resulting in the formation of other callus tissue around the first when vegetation resumes. Repetition of this annual process leads to the creation of a large target-shaped canker, with sinuous borders but an approximately ellipsoid shape, formed of a cracked central concavity surrounded by blackish, concentric callus folds, which is similar to cankers caused by Nectria galligena Bres. on P. tremuloides. After some years, the degraded cortical tissues peel to reveal rings of dead xylem, but the death of a tree is a rare event.
Secondary symptoms, occasionally observed on the foliage of P. tremuloides, take the form of blackish angular notches that preferably form near the vascular bundles, and of a necrosis of young shoots following the passage of the fungus via the petioles.
The typical teleomorph fruiting bodies form on the edges of cankers, in tissue dead since at least one year. They are black perithecial ascomata that burst out on maturity, with a characteristic long neck, and whose surface sometimes bristles with conidiophores (Table...). The one-celled, hyaline and hat-shaped ascospores are released in mucilaginous masses and can be disseminated by meteoric agents or insects (usually sap beetles of genus Epuraea Er.). The anamorph is ascribed to Chalara (Corda) Rabenh. (previously assigned to Thielaviopsis Went) and has three one-celled conidial forms, generated by single conidiophores or grouped in synnematal conidiomata: hyaline cylindrical conidia (8.5-32.8 × 2.7-7.5 µm), hyaline or brown barrel-shaped conidia (6.4-13.0 × 4.0-9.6 µm), and brown, thick-walled ovoid conidia (7.0-24.0 × 5.1-15.2 µm). They are produced on the infected bark or (especially the cylindrical type) in the underlying vascular tissues.
The parasite colonises the phloem and the xylem below the infected bark, both inter- and intracellularly, in which case it spreads through both the pits and the perforated plates. Resistant genotypes block further diffusion of the fungus at an early stage by differentiating cork and callus layers at the edges of the infected zone, together with cells containing tannic substances with an inhibiting action. The resistance response would also seem to be correlated with the concentration of growth hormones (auxins, cytokinins) in the plant, though the nature of this link has not yet been established. Inoculation tests with isolates from other broad-leaved plants on susceptible poplar clones, resulting in a limited degree of development of their cankers, revealed a certain, though not absolute, specificity in the relationship with the host.
Other Ceratocystis species, all encountered sporadically and almost solely on P. tremuloides stands in the Rocky Mountains and Alaska and of negligible phytopathological importance, are associated with cankers or dead bark zones. The possibility that some may be secondary invaders of cankers already produced by C. fimbriata cannot be ruled out.
_____
Other agents of cankers or bark alterations on poplars, whose incidence is more local and/or secondary, are the following:
- Nectria galligena Bres. (fam. Hypocreaceae, ord. Hypocreales, phylum Ascomycota), with anamorph Cylindrocarpon mali (Allesch.) Wollenw., a polyphagous parasite widely distributed throughout the northern temperate zone on fruit trees and forest trees, observed sporadically on poplar mainly in central Europe (Germany, Hungary) and in the Rocky Mountains; in this region, it can cause on P. tremuloides cankers with very evident calluses that can only be distinguished from those of Ceratocystis fimbriata by isolation of the fungus or by the appearance of its reddish fruiting bodies on cankers;
- Rhytidiella moriformis Zalasky and R. baranyayi Funk et Zalasky (fam. Cucurbitariaceae, ord. Dothideales, phylum Ascomycota), agents of a syndrome known as rough bark or cork bark on P. balsamifera and P. tremuloides respectively in western and central Canada; both are responsible for a gradual thickening of the entire bark of trunks and branches more than two years old, due to the death of the surface layers and abnormal proliferation of the underlying phloem, with the formation of corky ridges separated by deep fissures and progression to a greyish colour; R. moriformis also has an anamorph referable to Phaeoseptoria Speg., which appears on two- to five-year-old bark, followed by the teleomorph two or three years later;
- Diplodia tumefaciens (Shear) Zalasky, the anamorph of Keissleriella emergens (Karst.) Bose (fam. Lophiostomataceae, ord. Dothideales, phylum Ascomycota), which wasreported on P. tremula in northern Europe but is much more widespread in Canada and the northern U.S.A. on P. tremuloides and P. balsamifera; by contrast with the Rhytidiellae, it attacks small areas of the bark, where it causes an alteration similar to rough bark, and may also infect one-year-old branchlets and the main roots near the trunk (where the teleomorph sometimes differentiates); an additional symptom is the formation of distinct woody galls, due to hypertrophies of the bark and of the sap-wood induced by the fungus;
- Phoma exigua Desm. var. populi de Gruyter et Scheer (Mitosporic Fungi), an opportunistic parasite observed in the Netherlands in the 1990s and also the subject of earlier reports from Germany and Italy referred at the time to Phoma urens Ell. et Ev.; favoured by mild, damp winters, it causes cortical lesions on shoots and one-year-old branchlets of some P. nigra, P. × euramericana, P. × interamericana and P. trichocarpa clones which are quite similar to those provoked by Discosporium populeum, it is distinguishable, however, by the aggregated or confluent pycnidial condiomata and by their conidia, that are in part two-celled;
- Corticium salmonicolor Berk. et Br. (fam. Corticiaceae, ord. Stereales, class Basidiomycetes), a polyphagous species found in the tropics as the agent of so-called "pink disease" on eucalyptus, rubber tree, tea shrubs and other cultivated plants; in India, its incidence has recently been increasing in P. deltoides, P. × euramericana and P. yunnanensis Dode plantations exposed to high temperatures and humidity; its attacks on the trunk and branches often kill the main shoot;
- Dothiorella gregaria Sacc., the anamorph of Botryosphaeria dothidea (= B. ribis Gross et Dugg; fam. Botryosphaeriaceae, ord. Dothideales, phylum Ascomycota), an extremely polyphagous species (found on more than 100 genera of shrubs and both broad-leaved and coniferous trees) in the temperate zones and the tropics; it is able to attack plants already weakened by water stress or other diseases; on poplars, it is mainly active in north-central China, where it causes a bark necrosis on the trunk and branches, known as blister canker or ulcer disease, that develops rapidly in the spring and autumn and results in heavy production losses in the plantation;
- Botryodiplodia populea Z.K. Zong (Mitosporic Fungi), that has been observed over the last ten years in China, where it causes cankers on various poplar species, though its incidence is less than that of D. gregaria.
6 A regressive evolution of cankers has been reported on some P. trichocarpa clones in France: the necroses are quickly surrounded by vigorous callus tissues that prevented any further spreading.
7 The family is uncertain according to the Dictionary of the Fungi (op. cit.).
