Successions of Organisms in Discoloration and Decay of Wood [International Review of FORESTRY RESEARCH vol 2 page237-page 299 1967]

ALEX L. SHIGO

ALEX L. SHIGO

    A. Successions in Pulpwood and Pulp Chips.. 279
    B. Successions in Wood Products. 281
    C. Growth of Organisms in Wood Containing Natural Toxic
    Materials or Preservatives. 282
IX. Conclusions 283
    References 285

I. Introduction

Discoloration and decay of wood are the results of processes involving abiotic factors and organisms.  The role of organisms is emphasized in this review.
    In the laboratory it is possible for wood to be decomposed completely by one organism.  However, this is unlikely to occur in nature, where many organisms are competing constantly for nutrients and space.  The purpose of this paper is to review the literature relating to successions of organisms and the processes leading to discoloration and decay of wood.  Most papers contain but fragmentary accounts of successions.  An attempt is made here to bring together as many of these accounts as possible.  In most investigations on successions, examples are given for few organisms; usually it is stated that organism A followed organism B.  In a few cases, the appearance of organism C is mentioned.  No example of tracing a succession from initial infection to decomposition was found in the literature.
    Because successions of organisms proceed in a continuous manner, it is impossible to separate the events; there is always an overlap.  For purposes of organizing this review, however, it is necessary to separate the events into discrete sections, and some repetition was unavoidable.  An attempt was made to begin with events occurring in living trees and to follow successions until the tree is dead and cut into products.  Events occurring in living trees were emphasized because these appear to be the most complex.  The living tree exerts forces in these processes, whereas after the tree is dead, organisms compete only among themselves.  Yet most of the available examples of successions deal with dying and dead trees, and rates of deterioration are emphasized.
An ecological-physiological approach to successions is given. Organisms must be understood both as individuals and as parts of an ecosystem.  A thorough discussion of successions would entail discussions on many subjects related to physiology and ecology.  In this review many of these subjects are mentioned only briefly, mainly because so few investigations have been conducted on them.

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    Forest pathology emerged as a science in the latter half of the nineteenth century, one of the most eventful and turbulent periods in the history of the biological sciences.  The Ungerian period, based on the theory of spontaneous generation, was then nearing an end; and belief in the germ theory was increasing.  From 1853 to 1860 Pasteur conducted intensive research on the role of microorganisms in fermentation.  Strengthened by the research of Koch and others, the science of microbiology began to develop rapidly.  During this period some of the basic principles of plant pathology evolved: DeBary demonstrated in 1853 that fungi could cause diseases of plants; Burrill showed in 1878 that bacteria could also cause plant diseases; and in 1888 Beijerinck added viruses to the growing list of plant pathogens.  These monumental events firmly set the bases for the science of plant pathology.
    The descriptive phase of mycology was relatively well established by the middle of the nineteenth century.  By then the detailed structures of many fungi were known, particularly those that inhabit wood and produce large sporophores, the Hymenomycetes.
    Although forestry had an early beginning, it was not well recognized as a science until the latter half of the eighteenth century.  In Central Europe the science of forestry developed and reached a higher level than in any other area.  By the latter half of the nineteenth century an increasing population caused great concern for conservation and better utilization of wood.  Foresters had an increasing concern for forest trees; mycologists were becoming better acquainted with Hymenomycetes; and the basic principles of plant pathology were developing rapidly.  The occurrence of all these events at approximately the same place and time set the stage for the emergence of forest pathology as a science. 
    Some people regard Theodore Hartig as the father of forest pathology because of his early investigations of hyphae in wood.  Hartig, an adherent to the Ungerian School, concluded that decay was responsible for fungi.  In 1874, Robert Hartig took the opposite side.  He disproved the spontaneous generation theory of fungi in wood and showed that fungi cause decay.  As a result of these studies he is regarded by most people as the father of forest pathology.  But Robert Hartig himself regarded his contemporary, M. Willkomm, as the founder of the science (Hubert, 1931).  Willkomm, a German botanist, studied hyphae in wood and published a well-illustrated book, "Die Mickroskopischen Feinde des Waldes," in 1866.

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The research of Robert Hartig stimulated many other investigators to study decay.  The studies that followed were all based on the principle that fungi-meaning only Hymenomycetes-could decay wood.  Most early studies dealt primarily with damage caused by fungi.  In Europe the increasing demand for wood products stimulated studies related to utilization and products pathology.  In the United States, because of the vast and seemingly endless virgin forests, the emphasis was on studies of cull and pathological rotation.  During this period, taxonomic investigations were continued by mycologists.
    To this day taxonomy of decay fungi., cull studies, and products pathology have continued to be the major concern of research.  Indeed the principles of decay, as stated by Robert Hartig, have been altered very little.  An excellent review on decay is given by Wagener and Davidson (1954).
    Only recently has some attention been given to organisms other than Hymenomycetes in decay processes.  These recent studies suggest that many different organisms are involved in the processes that result in decay. 
    Investigations of discolorations have dealt primarily with blue stain caused in conifers by species of Ceratocystis.  Robert Hartig in 1878 stated that blue stain in conifers was caused by species of Ceratostoma (Ceratocystis).  Willkomm had seen these fungi in 1866, but he considered them as rot fungi.  Von Schrenk (1903) and Hedgcock (1906) made many valuable early contributions to the knowledge of blue stain.  Von Schrenk described a blueing process in many species of conifers.  Hedgcock showed that several other fungi also stained wood.  Lagerberg et al. ( 1927) added many fungi to the list of wood stainers.  Scheffer and Lindgren (1940) added more, but devoted most of their attention to stains in wood products. 
    Conifers, wood products, blue stain, and species of Ceratocystis still dominate investigations of discoloration.  Little work has been done on hardwoods, especially on the discoloration processes in living trees.  Discolorations initiated by wounds and aggravated by organisms were neglected in investigations because the discolored tissues were considered to be either true heartwood or a special type of it.  But recently interest has increased in discoloration in living trees and the relation of discoloration to decay. The role of bacteria in discoloration is also being investi- gated.  In some species of trees, decay fungi appear to invade only those tissues that have been previously invaded by bacteria and non-Hymenomycetes.

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III. Basic Information on Ecology and Physiology Pertinent to Successions

1. SUCCESSIONS AND A DYNAMIC ENVIRONMENT

In many ways the successions of organisms involved in discoloration and decay of wood are similar to successions of higher plants on soils.  But care must be taken not to pursue the similarities too far.  Successions of green plants usually are considered as steps in building toward climax societies, while successions of microorganisms in discoloration and decay of wood are degradation processes.
    Freshly exposed wood on a living tree may be compared to land stripped of all plants. Pioneer species invade both sites.  The processes are most comparable in dead trees, where it is often possible to observe the effects of nutrients and environment on the organisms.  But on living trees a more dynamic situation is encountered.  New wood is being formed by the cambium at the same time that older wood in the interior of the tree is being decomposed.  Good accounts of green plant ecosystems and general information on this subject are presented by Ovington (1962).  Successions of forests and diseases in the forest have been studied by Baxter (1937), Baxter and Wadsworth (1939), and Baxter and Middleton ( 1961 ) .  They explain that, as forests change, successions of disease result.  Changes of forest type are accompanied by changes in temperature, moisture, substrates, and other conditions. Organisms must adapt continuously to these changing conditions if they are to survive.  The type and rate of successions are greatly effected by changing conditions.  Such ecological adaptations in fungi have been studied by W. Brown and Wood (1953).  Many publications on ecology of fungi are reviewed by Cooke (1948, 1951, 1953), and the subject is discussed by Williams and Spicer (1957).

2. ASSOCIATIONS AND INTERACTIONS

    D' Aeth (1939) stated that "successional diseases may occur on the living host through the action of one fungus in developing a substrate which is more favorable for a second fungus, a process comparable to the successive metabolic stages of decay under natural conditions.  Frequently, one parasite by its attack on a plant allows the entrance of a more virulent parasite, which could not by itself have initiated the attack."  An example is cited: Scleroderris fuliginosa can infect twigs and shoots

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of Salix fragilis that has first been infected by Cryptomyces maximus and other fungi.  Later a third fungus, Myxosporium scutellatum, infects and aggravates the disease complex.
    D' Aeth (1939) emphasized that pure cultures are rare in nature.  Therefore, as successions continue, repeated associations and interactions of organisms occur.  The most aggressive organism continues to invade and to alter the substrate.  Eventually the substrate is altered sufficiently to permit invasion by different organisms, which must first associate and then interact before the most aggressive organisms continue to invade.  This cycle continues until the substrate is decomposed. 
    As organisms grow toward each other in wood, the hyphae enlarge and darken, and dark substances often form in the wood cells (D' Aeth, 1939).  This serves as one explanation for the dark lines-zone lines- found in columns of decay (A. H. Campbell, 1933; Hopp, 1938). 
    Barlund (1950) and Lehmann and Scheible (1923) studied interactions of decay fungi on wood blocks in the laboratory.  Barlund pointed out that, when certain wood-inhabiting organisms invade the wood first, they may prevent others from invading by removing from the wood substances necessary for their growth.  She also suggested that species with rapidly growing surface mycelium have an advantage in the early stages of colonization. However, Lehmann and Scheible showed that inoculations of wood with Coniophora cerebella increased the rate of growth and decay by Merulius lacrymans and Stereum purpureum.  The non-Hymenomycete Coryne sarcoides retarded considerably the decay by Coniophora puteana and Polyporus tomentosus in laboratory experiments (Etheridge, 1957).  These studies suggest that pioneer organisms may be important agents in determining the type and rate of decay that follows. 
    Westerdijk (1949) gave many examples of associations, and she thought the word "associations" should be used more frequently, and that more attention should be given to natural associations.  One example she presents is wood pulp in which "a very special association, comprising Phialophora species and yeast-like fungi of the genus Hyalodendron, occurs."  In decaying wood, she mentions Trichoderma viride as being followed and later joined by Penicillium spp.  Because some organisms are often associated closely in wood, it is difficult to determine how far the succession has progressed.  One organism may invade first, and then be joined by another, as in the example given for Trichoderma viride and Penicillium spp.  Similarly, Hypocreopsis lichenoides and H. rhododendi

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are often associated with Hymenochete spp. (Cauchon and Ouellette, 1964). 
    In conifer needles, Naevia piniperda (Sarotrochilia piniperda) and Lophodermium macrosporum are often associated (Lagerberg, 1928).  Darker (1964) gave another account of such an association, but included additional information on a succession.  The primary invaders of the needles of Abies balsamea studied were Hypodermella mirabilis and Bifusella faullii.  Secondary fungi invaded about a year after the primary infection when the pycnidial stages were maturing.   At this time the needles were still firm, and starch was abundant in the mesophyll cells.  The principal secondary invaders were Stegopezizella balsamae (Sarcotrochila balsamae), Lophodermium autumnale, and Leptosphaeria faullii.  These fungi competed for the rich supply of nutrients in the needles.   And, when the secondary fungi occurred in abundance, they prevented maturation of the hysterothecia of the hypodermataceous species.  Invasion by secondary fungi often destroys evidence of primary invaders.

1. ROLE OF ENZYMES

    Physiological factors are the basis for successions.  To be specific:  Enzymes are the crux of this discussion.  A substrate is made available, and the digestion of it begins.  As many environmental factors affect the substrate, organisms with enzymes capable of digesting it under the prevailing conditions are able to survive.  Factors that affect these enzymes then affect the successions.  The basic principles of parasitism also may be explained at the enzyme level (Barnett, 1959). 
    Physiological studies of many species of fungi have given valuable information about the factors that affect growth, reproduction, sporulation, and the like (Lilly and Barnett, 1951; Cochrane, 1958; Jennison et al., 1955).  Deficiencies in many organisms may account for their dependence on other organisms to supply needed substances.  For example, many Basidiomycetes are deficient, or heterotrophic, for vitamins, especially thiamine (Robbins, 1950; Robbins and Hervey, 1955, 1958).  These fungi cannot compete successfully on a deficient substrate, so they must wait until the substrate is altered.  On the other hand, some organisms grown on particular substrates may leave behind substances that are toxic to other organisms. 
    Some organisms also may be held back by substances produced by the

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tree itself.  As organisms invade deeper into the wood of living trees, they are confronted increasingly by many types of substances produced by the trees, such as gum and resins (Frank, 1895; Higgins, 1919; Rankin, 1933; Neger, 1924; Kuster, 1925; Swarbrick, 1926; Bloch, 1941).  These materials and the tissues containing them sometimes function as barriers to invading organisms.  Indeed, resistance is the rule and infection is the exception in nature (W. Brown, 1934).  Yet some organisms do digest these materials.  Examples are given later of organisms that can grow on wood containing a wide variety of toxic materials.  Needless to say, the capacity of a fungus to survive here depends on its enzymatic capabilities.
    A review of enzymatic degradation of cellulose and wood is given by Cowling (1958).  The microbial decomposition of cellulose is discussed in detail by Siu (1951), and the degradation of lignin is discussed by Cooke (1957).  Liese and Schmid (1962) found that cellulases occur in advance of the hyphae.  The nature and interplay of enzymes produced by various organisms are basic to their relative position and influences in a succession.

2. MYCOPARASITISM

Successions are not always direct routes-often they entail many detours and sideroads.  Yet all paths are directed toward decomposition of the substrate.  The organisms involved in successions are constantly competing with one another for space and nutrients; and even as they compete they are themselves under constant attack from other organisms that find them good substrates for growth.  Fungi that attack other fungi are termed mycoparasites.  Mycoparasites complicate successions because they increase competition and tend to weaken fungi that are competing for the wood.  Excellent reviews on mycoparasitism are given by Barnett (1963, 1964). 
    Several examples of mycoparasitism of wood-inhabiting organisms are known.  Even though the exact effects of mycoparasitism on successions are not known, its existence should be recognized in a discussion of succession. 
    Two examples are listed by D' Aeth (1939): (1) Trichothecium roseum, Coniothyrium sp., and many other fungi grow on the stroma of Dibotryon morbosum on Prunus spp.; and (2) Tuberculina maxina occurs commonly on the spores of Cronartium ribicola on Pinus strobus.  Trichothecium roseum and Gliocladium roseum have been noted growing on mycelial mats of Ceratocystis fagacearum (Shigo, 1958) and on C. virescens

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(Shigo, 1962b) on pulpwood bolts.  Gliocladium roseum is a very aggressive fungus, and it will also attack mycelium and conidia of Trichothecium roseum (Barnett and Lilly, 1962).  Gonatobotryum fuscum attacks species of Ceratocystis and related genera (Shigo, 1960).  Gonatorrhodiella highlei is an aggressive mycoparasites on Nectria spp. (Ayers, 1941; Blyth, 1949; Shigo, 1964a).  Gonatobotryum fuscum and Gonatorrhodiella highlei are similar in their mode of parasitism (Shigo, 1964a).
    Barnett (1964) mentions unpublished data on some wood-rotting Basidiomycetes thought to attack other wood-inhabiting fungi.  Griffith (1964) later stated that endoconidia of Ceratocystis spp. were highly susceptible to attack by certain Basidiomycetes, and that their mode of attack is similar to that of Rhizoctonia solani and Gliocladium roseum. 
    Sporophores attacked by other fungi are common sights in the forest.  Nonhymenomycetous fungi and bacteria are the principal invaders.  Yet, some species of the Agaricaceae attack others in the same family-for example: Volvaria loveiano on Clitocybe nebularis, Stropharia coprinophila on Coprinus atramentarius and Nyctalis, and Claudopus sp. on Polyporus perennis (Fitzpatrick, 1915). 
    Valuable information about the basic principles of parasitism has been obtained from investigations of mycoparasites.  Host nutrition and environment greatly affect the degree of parasitism.  These results also contribute to an understanding of why different organisms enter successions as substrates are altered.

IV. Successions of Organisms in Discoloration and Decay
    Processes in Living Trees, Especially Hardwoods

A. General Discussion

The surface bark on healthy living trees abounds with a wide variety of organisms.  Although lichens, algae, and mosses are the most conspicuous organisms on bark, microorganisms are by far the most abundant (Bier and Rowat, 1962a,b, 1963; Bier, 1963a,b).  Most microorganisms are saprophytes and cause the tree no injury.  Indeed, under some circumstances these organisms can actually benefit the tree by protecting it from aggressive parasitic organisms (Bier and Rowat, 1962a,b, 1963; Bier, 1963a,b ).   Bark moisture is an important factor affecting the invasion of bark parasites and the action of bark saprophytes on these parasites.  As bark moisture is reduced, conditions favor the parasites (Bier, 1959, 1961a,b,c, 1964).

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    When any agent reduces tree vigor [Note from webmaster: better defined as vitality and not vigor - JAK2004], wood-inhabiting organisms gain the advantage.  Some pioneer wood-inhabiting organisms are present in an inactive state on the bark of living trees. 
    Wood-inhabiting organisms-bacteria and fungi-are emphasized in this section.  Most of these organisms require weakened or exposed tissues as infection courts.  Infection courts occur when mechanical injuries, death of branches, or other agents kill bark and disrupt the living bark-wood interface.  Once this occurs, a new and abnormal wood-atmosphere interface is formed.   Tissues are exposed to atmospheric conditions for the first time-suddenly, as when a mechanical wound is inflicted; or gradually, as when a branch dies because of a combination of factors. 
    Immediately after exposure an exchange of air and moisture takes place between cells and atmosphere.  The physiological processes in the exposed cells are affected by the new environment.  These processes in living but injured cells result in the formation of certain substances, some of which-especially phenolic compounds (Erdtman, 1939; Farkas and Kiraly, 1962)-are formed by dying or injured cells (von Rudloff and Jorgensen, 1963).  These substances are considered to afford protection against invading organisms, and the tissues around wounds that contain the phenols are known as protection wood (Frank, 1895; Zycha, 1948; Jorgensen, 1962).  In some trees the protective zones apparently wall off invading organisms (Hepting and Blaisdell, 1936; Shigo, 1965b), while in other trees the protective zone, if present, is not effective (Shigo, 1966).
    If the protective barriers were effective in every case, there would be little or no internal defect in trees.  Conversely, if the protective barriers were never effective, there would be little or no sound wood in trees.  The great variation in extent of discoloration and decay in living trees is indicative of the many factors that influence these processes.  Three general conditions that may account for this variation include the following: (1) The protective barrier may not be formed, either because of environmental conditions or because of the conditions of the injured cells; (2) the protective barrier may be formed, only to be penetrated by particularly aggressive organisms; or (3) the protective barrier may be formed and function effectively. 
    Discoloration may occur in the absence of microorganisms.  To what extent such processes can continue is not known.  Organisms are associated frequently with discolored tissues, but their role in the discoloration process is not completely clear.  It is known that tissues formed after a tree is wounded are seldom discolored. Because organisms infect primarily the discolored tissues, they rarely infect the tissues formed subsequent to

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wounding.  Bacteria and nonhymenomycetous fungi usually are the first organisms to invade the discolored tissues.  The Hymenomycetes follow; and, like the bacteria and non-Hymenomycetes, their development is restricted to the tissues originally discolored.  The succession of organisms in living trees does not end with the invasion by the first decay fungus; other decay fungi often follow.  A good example of this is presented by Nobles and Nordin (1955) for Corticium vellereum in sugar maple.  This fungus was isolated from many different types of decay by Nordin (1954), and it was learned later that it followed other decay fungi.  Eslyn (1962) reported a similar situation with this fungus and silver maple (Acer saccharinum) and stated that the fungus Trechispora brinkmanni may be similar to C. vellereum in this way.

B. Heartwood and Related Tissues
    Although a good understanding of the processes leading to formation of heartwood and related tissues is a necessary prerequisite to an understanding of discoloration and decay, only literature pertinent to succession will be discussed here.     
    Heartwood, false heartwood, and other terms have been used loosely in some publications.  This has resulted in some confusion, especially with regard both to the nature of discoloration and to the successions of organisms.  The discolored tissues associated with wounds are often termed heartwood or a type of heartwood.  Sandalwood "heartwood" has been induced by injecting materials into trees.  Kadambi (1954) reported: "The same results may sometime be achieved by making bore holes through the trees, but heartwood formation is generally confined in such cases to the vicinity of the bore holes.  Traces of heartwood formation can also be induced by injury treatments like root pruning, lopping and sometimes by dealing mechanical blows oil the surface of the trees which jam the superficial tissues.  " What is called heartwood in this case is similar to the discolored tissues associated with increment borer wounds and other mechanical wounds.
    Even though organisms may not initiate the discolorations, they may aggravate the discoloration processes, especially in species such as Fagus silvatica, in which formation of tyloses is associated with the slight discoloration. Jurasek (1959) stated: "The presence of fungal infection in wood cannot be considered to be a necessary condition for the growth of tyloses and their formation because tyloses are formed even in sterile wood. However, fungi can indirectly affect the formation of tyloses as they damage the living tissue." Necesany (1959) pointed out that heart- 

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wood formation is a physiological process in all tree species, where the parenchyma cells die either by natural aging or from the influence of environment with simultaneous formation of tyloses and heartwood substances. 
    The importance of fungi in discoloring processes cannot be discounted completely (Good et al., 1955).  Busgen and Munch (1929) stated that ultimately there appears to be no difference between tissues temed false heartwood and heartwood.  Yet, differences must exist, because while organisms readily infect those discolorations (often termed false heart- wood or pathological heartwood) associated with wounds, they rarely infect the true heartwood (Shigo, 1965b). 
    Some good accounts exist of heartwood formation and related processes that are pertinent to this subject (Busgen and Munch, 1929; Zycha, 1948; Chattaway, 1952; Paclt, 1953; Bosshard, 1953; Krzysik, 1954; Harris, 1954; Good et al, 1955; Buchholz, 1958; Frey-Wyssling and Boss- hard, 1959; Jorgensen, 1962). 
    A good account of a succession of organisms associated with heartwood in Thuja plicata was given first by Eades and Alexander (1934) and later by Findlay and Pettifor (1941).  Dark and light heartwood occur in this species.  The dark heartwood contained non-decay fungi, but no organisms were found in the light heartwood.  Findlay and Pettifor concluded that the fungi probably were responsible for the dark heartwood and the reduced strength and specific gravity of that wood.  They observed hyphae in the cells and at first thought it to be Poria weirii, a common pathogen of T. plicata.  They cited the work of McCready (as quoted by Boyce, 1961) as their basis for this conclusion. Actually, however, what McCready described was not P. weirii but hyphae of non- hymenomycetous fungi (Roff, 1964).  This supports the conclusions of Findlay and Pettifor that the fungus in the dark heartwood probably was not a decay fungus. 
    Findlay and Pettifor also report results from laboratory tests showing that test blocks of this dark heartwood were susceptible to attack by certain decay fungi such as Coniophora cerebella, whereas it was with great difficulty that fungi could be induced to grow at all over the light colored heartwood.  This suggests a succession in which C. cerebella follows non-hymenomycetous fungi. Shigo (1965b) has pointed out that discolorations which often form in sapwood and are later included in true heartwood are difficult to see because of the dark color of the true heartwood in some species.  It is here, however, in these darkest tissues, and not in the light-colored heartwood tissues, that successions of organisms occur.

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C. Discoloration and Decay in Populus spp. with Special Reference to Fomes igniarius

Some of the most extensive studies on organisms involved in the discoloration and decay of living trees have dealt with Populus spp. in Canada and the United States.  The major organism associated with decay in Populus spp. is F. igniarius var. populinus.  This fungus and its varieties are important white rotters of hardwoods, particularly species of Populus, Fagus, Betula, and Acer (Ohman and Kessler, 1964).  The fungus produces large, conspicuous perennial sporophores on living trees-which facilitate locating study trees.  The many accounts of this fungus and of other organisms in Populus spp. add to our knowledge of successions.  One of the best accounts of organism succession in the discoloration and decay of living trees is given by Etheridge (1961), who studied the factors that affect branch infections in aspen (Populus tremuloides).  He considered the relative frequency of isolations of the organisms from branches dead for known periods of time as an indication of the probable course of succession.  Five distinct stages of colonization in aspen branches were described.  
    Stage 1. Bacteria were the first organisms to colonize the branches.  Isolation of bacteria from branches that had been dead for periods up to 22 years indicated that there had been no general replacement of this group by later groups of colonizing fungi. Bacteria showed no preference for specific parts of the sample trees and were found in association with several different species of later-colonizing fungi. 
    Stage 2. Colonization by fungi did not occur until 4 years after the death of branches.  Cytospora spp. were the principal fungi of this stage.  
    Stage 3. After 6 years, Cytospora chrysosperma, Phoma sp., Libertella sp., and several other species of fungi were isolated frequently.  Cytospora chrysosperma was the most aggressive colonizer.
    Stage 4. Corticium polyonium and Polyporus adustus two wood- destroying fungi, were isolated from the branches after 8 and 9 years. 
    Stage 5. Fomes igniarius was isolated from branches dead 19 years or more. 
    These results suggest that bacteria are some of the first to invade, followed by non-decay fungi, and then by decay fungi.  No attempt was made in this study to identify the pioneer bacteria. 
    An earlier account of decay in Populus tremuloides and P. grandidentata, caused by Fomes igniarius var. populinus, is given by Riley ( 1952), who stated that in these species discoloration of otherwise ap-

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parently sound wood is common.  A dull reddish stain appeared typically around knots caused by dead branches.  Discolorations invariably were associated with wounds.  Heartwood was discolored frequently to various shades of dull red, brown, and olive green, often intermixed.  The discolored region sometimes extended for considerable distances above or below typical decay caused by F. igniarius var. populinus.  This fungus was not obtained farther than 2 or 3 inches from visibly decayed wood longitudinally, or approximately 1/4 inch laterally.  Numerous cultures on agar from discolored wood indicated the presence of various fungi and bacteria.  Two fungi were identified as belonging to the genera Torula and Corticium.  No attempt was made to identify the other organisms. 
    Johnson et al. (1930) stated that they saw no fungi in the discolored tissues around decay.  Etheridge (1961) and Basham ( 1958a ) listed Corticium polygonium as an aggressive decay organism.  The results obtained by Riley (1952) indicated clearly that Fomes igniarius var. populinus and possibly other decay fungi advanced through tissues that already were discolored and already contained bacteria and non-decay fungi. 
    In his discussion Riley stated that the presence of heartwood was not a necessary prerequisite for attack by Fomes igniarius var. populinus and that-according to the results of inoculation experiments-the fungus, was capable of infecting and causing typical decay in sapwood.  Significantly, associated with the inoculation wounds was a zone of reddish- brown discoloration in the sapwood, from which numerous organisms were isolated.  These results indicate that, indeed, F. igniarius var. populinus does not infect true heartwood, but does infect tissues erroneously termed true heartwood that were discolored, first through ,the action of abiotic factors, and later by non-decay organisms. 
    Therefore, from the standpoint of succession, it is important to distinguish true heartwood from wound-initiated discoloration (Shigo, 1965b ).  If wound-initiated discoloration is considered true heartwood, then an invading decay fungus would be considered a pioneer invader and the formation of true heartwood would be considered prerequisite for invasion.  On the other hand, if wound-initiated discoloration is understood to result from interactions of external factors and non-decay organisms, then the successional pattern in discoloration and decay in living trees becomes clear: discolorations caused by abiotic factors and non-decay organisms often are followed by decays caused by Hymenomycetes.
    Additional information on the subject is given by Basham (1958a, 1960), who cut and examined 1754 Populus tremuloides trees in Canada.

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Two distinctly different discolorations were encountered.  One was a light brown to grayish brown; the other was red, often mottled.  A species of Libertella was frequently- associated with the latter.  Phialophora alba and other members of the Fungi Imperfecti also were associated with the discolorations.  These organisms were also isolated from the discolored tissues that surrounded decayed wood.  Basham stated that, in the trees sampled, the heart rots invariably were surrounded by discolored wood, usually brown.  The red mottled discoloration occasionally replaced brown discoloration in this association, and frequently the red mottled discoloration mixed with the extensive brown discoloration that was nearly always present at stump height.  In many mature and overmature defective trees, this mottled discoloration was the sole interior defect in the small top logs.  The solid core of discolored tissues near the crown, and the" band of discolored tissue yielding non-decay organisms from around decayed wood, revealed again the familiar successional pattern.  Many figures in Basham's (1958a, 1960) publications illustrate these points clearly, especially the decay surrounded by firm but discolored wood. 
    The presence and importance of non-decay organisms was pointed out by Thomas et al: (1960) when they stated that a large number of infections in Populus spp. which had resulted in rot could not be connected with fungi of known decaying ability.  Thus they did not identify the organisms associated with 47% of the decays recorded, largely because the mycoflora was dominated by non-decay fungi.  Too often these "other organisms" are not even mentioned in publications, and consequently little is known about them.  But their presence is known to all who have isolated organisms from discolored or decayed wood.  An early account of these other organisms in Populus spp. is given by Schmitz and Jackson (1927), who also mentioned similar studies by European investigators.  Why wood is invaded by Fomes igniarius var. populinus only after other organisms have first invaded and altered it is not understood completely, although the factors known to affect spore germination shed some light on this subject.  While spores of F. igniarius germinate poorly on water agar and only reasonably well in a solution of glucose and maltose, they germinate well on malt extract agar and on old wound surfaces ( Good and Spanis, 1958). 
    Good and Spanis (1958) stated that the most clear-cut change in the nature of the wound surface is the rather rapid drop in pH from 6.0 to finally 4.5 or 5.0.  They suggest that wound saprophytes may be responsible for this change.  Therefore, unlike fungi such as Fomes annosus and

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Stereum spp., which require a fresh substrate for infection (Brooks and Moore, 1926; Rishbeth, 1950), F. igniarius requires a substrate that has been colonized earlier by other organisms. 
    The most comprehensive study on the variety of organisms associated with decay in living species of Populus was conducted by Good and J. I. Nelson (1962).  This study gave much excellent information about successions, with emphasis again on Fomes igniarius var. populinus.  Of 64 species of fungi isolated, the most common were members of the following genera: Alternaria, Candida, Cephalosporium, Chaetomium, Coniochaeta, Coniothyrium, Cytospora, Dicoccum, Epicoccum, Haplographium, Hormodendrum, Illosporium, Mucor, Penicillium, Phialophora, Phoma, Pullularia, Trichoderma, Tritirachium, and Verticillium.  The decay fungi Isolated most frequently were Fomes igniarius, Hericium sp., Stereum sp., Radulum sp., and Phlebia sp..  Bacteria also were isolated frequently; but, as in many studies, they were not identified. 
    Good and J. I. Nelson (1962), who had anticipated a more regular succession of organisms, interpreted their results to show no evidence of such a sequence.  Although they concluded that no regular succession was obvious, they reported that the wood into which Fomes igniarius var. populinus progressively grew had, in most cases, already been colonized by other fungi, including a number considered to be saprophytes.  They showed that the fungi from trees without decay were similar to those found in discolored tissues or the incipient decay associated with F. igniarius var. populinus.  This suggested that these fungi did not follow the decay fungi but came first, and that they rendered the wood suitable for invasion by F. igniarius var. populinus.  Good and J. I. Nelson (1962) concluded that F. igniarius var. populinus is not a primary invader and must follow other organisms. 
    In a similar study with other tree species, Shigo (1963b) demonstrated the same successional pattern.  From 2400 isolation attempts made from 59 trees infected by Fomes igniarius, only a few species of non-decay fungi predominated: Phialophora spp., Hypoxylon spp. (Acrostaphylus imperfect stages), and Trichocladium canadense.  Bacteria were isolated frequently from almost every tree.  Bacteria were isolated from the tissues that yielded non-decay fungi, and these organisms grew well together in culture.  Fomes igniarius grew through tissues discolored first by abiotic factors and invaded subsequently by other organisms; it invaded the discolored tissues but not the narrow zone of firm discolored tissue next to the white wood.  This discolored tissue continued to yield bacteria and other fungi, even around the oldest decayed tissues.  The

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data were interpreted to indicate that three kinds of organisms are important in bringing about the decay processes: bacteria, non-decay fungi, and decay fungi.

    Wounds through the bark expose sapwood, and also heartwood if the wound is deep enough in those trees possessing such tissues.  When a branch dies, the center of the tree is opened to attack by microorganisms.  Because branch wounds are more common than other wounds, the central area of the tree receives the greatest threat of invasion. 
    Branch stubs are often regarded as the most significant infection court on many species.  Such was the case in a study with red maple (Acer rubrum) in the northeastern United States (Shigo, 1965a).  In this study, involving more than 10,000 isolations, Shigo demonstrated a succession of organisms in red maple sprouts.  Bacteria were the first organisms to colonize wounds, and nonhymenomycetous fungi followed soon after.  Bacteria were intimately associated with those fungi in wood tissues, and the bacteria and fungi grew well together in culture.  The principal pioneer fungi were Phialophora spp. (P. melinii was most frequent), Trichocladium canadense, Hypoxylon spp., and Cytospora decipiens.  The bacteria and some of the pioneer fungi isolated from discolored tissues surrounding decay columns inhibited in culture the growth of Hymenomycetes isolated from the decay columns (Shigo, 1966). 
    These studies and others by Shigo (1963b, 1965a,b) described the pattern of discoloration and decay in living trees and illustrate successions of organisms.  Discolorations form soon after bark is ruptured.  These discolorations, although initiated by abiotic factors, are enhanced by organisms.  Bacteria and nonhymenomycetous fungi preceded the Hymenomycetes.  The wood tissues that formed after the branch died, or after the wound was inflicted, were seldom discolored or decayed.  Two common exceptions to this pattern resulted from invasion by Poria obliqua and Polyporus glomeratus.  But these fungi still grew only through tissues already invaded by other organisms.  Discolored tissues that yielded bacteria and the pioneer nonhymenomycetous fungi surrounded the decay. 
    The two Hymenomycetes mentioned above formed sterile growths of hard, black fungus material in the infection courts.  As new tissues around the infection court were invaded, the decay remained surrounded by dis-

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colored tissues that yielded other organisms.  These discolored zones are often referred to as incipient decay, yet Good and C. D. Nelson (1951) were unable to show that P. glomeratus occurred either in the dark zones surrounding decay or in the dark tissues above the typical decay.  The occurrence of many non-Hymenomycetes in these discolored tissues in Acer saccharum was pointed out by Nordin (1954).  The dark zones usually are very moist and have a high pH.  These factors may limit the radial growth of Hymenomycetes in wood (Shigo, 1965b). 
    Mechanical wounds usually exposed sapwood.  This may explain why fungi not commonly found in trees of virgin stands are found in trees in stands that have been logged. ( Baxter and Hesterberg, 1958).  The type of wound is an important factor affecting the succession that follows.  For example, Nordin (1954) did not find P. glomeratus associated with frost cracks even though such cracks were the most important infection court in Acer saccharum in his study area.  On the other hand, this fungus commonly infects branch stubs. 
    Hypoxylon spp. are pioneer fungi which commonly infect exposed sapwood (Shigo, 1966).  Species of Hypoxylon and some other members of the Xylariaceae are unique, for they are Ascomycetes that decay wood (Merrill et al., 1964).  Members of the genus exhibit a wide variety of action against trees.  While some Hypoxylon species are pioneer fungi, others are the last organisms to digest the wood after attack (W. A. Campbell and Davidson, 1940b). Some species are very aggressive parasites, such as Hypoxylon pruinatum on Populus spp. (Berbee and Rogers, 1964), Hypoxylon tinctor on American sycamore (McAlpine, 1961), and Hypoxylon spp.   (Ustulina vulgaris) on other tree species (Wilkins, 1935, 1939, 1943).  Some species often are associated with Hymenomycetes in living trees (Ferdinandsen and Jorgensen, 1938-1939; Bakshi et al., 1956; Shigo, 1966), especially with species of Stereum (W. A. Campbell and Davidson, 1940a). 
    Stereum spp. are some of the most aggressive pioneer Hymenomycetes; they commonly follow Hypoxylon spp. and apparently grow in close association with them in living trees (Ferdinandsen and Jorgensen, 1938- 1939; Shigo, 1966).  Much of the information about Stereum spp., especially S. purpureum, comes from studies of silver-leaf of Prunus spp. (Brooks and Moore, 1926).  In these studies it was shown that S. purpureum successfully invaded freshly exposed tissues.  If tissues were exposed to air for long periods, other microorganisms frequently invaded them first.  These other fungi were thought to alter the nutritive condition of the wood sufficiently to preclude S. purpureum. Stereum purpureum

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was not able to invade successfully tissues first inoculated with Sclerotinia cinerea and Diaporthe perniciosa.  These results suggest again that the pioneer organisms often determine the successional pattern.

2. DISCOLORATION AND DECAY FOLLOWING INCREMENT BORINGS

    Successions of organisms following wounding are illustrated vividly in studies of increment-borer wounds (Lorenz, 1944; Hepting et al., 1949; Toole and Gammage, 1959). Lorenz (1944) reported the following results from different tree species wounded 1 and 2 years previously.  In Betula papyrifera, the wood above and below every borer hole, whether plugged with a wooden dowel or not, was stained reddish brown from 2.5 to 4.5 feet; no decay was visible around the holes; and the fungi isolated were typical wound saprophytes.  In Betula alleghaniensis, a reddish-brown stain was associated with all the borer holes.  The stain usually extended 3 to 4.5 feet above and below the hole (maximum 6 feet); fungi and bacteria were isolated consistently from the wood; and decay caused by Hymenomycetes extended 3 to 18 inches up and down from 4 of the 24 holes in three check trees, and from 1 hole in the treated trees.  In Tilia americana, the wood around all holes, regardless of plugging, was stained a uniform dark gray; the stain extended an average of 6 inches above and below the plugged holes, but slightly farther above.  Below the unplugged holes decay was associated with 22 of the 88 holes and averaged about 1 X 2 1/4 inches in extent.  In Acer saccharum, a salmon-colored stain that often had dark green streaks near the margin extended about 6 inches above and below the holes.  Decay was associated with 10 of the 48 holes in the treated tree, the decay being greatest around the unplugged holes.  Isolations from the stained wood, as in the other three species examined, always yielded fungi, or bacteria, or both. 
    Because of additional experiments with freshly cut bolts, and earlier information about stored bolts (Bailey, 1910), Lorenz concluded that the discolorations were of a chemical nature even though organisms were constantly associated with them.  These results lend further support to the concept that discolorations can proceed for a limited time without organisms.  In living trees, however, the discolored tissues always were inhabited by organisms, and decay fungi were isolated only when these other organisms were present.  Some of the pioneer fungi isolated were in the same genera as those isolated from discolored tissues of other hardwoods: Torula, Conciochaeta (may be a stage of Phialophora; Rogers, 1965), Fusarium, and Alternaria (R. W. Davidson and Campbell,

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Toole and Gammage (1959) reported similar results for Quercus nuttallii, Fraxinus pennsylvanica, Celtus laevigata, Liquidambar styraciflua, and Populus deltoides.  Although they agreed in part with Lorenz on the cause of the discoloration, they added that the six discoloring fungi isolated were responsible for some of the discoloration.  Their data, showing that decay fungi were preceded by other organisms, constitute a good example of a succession in these tree species.  The decay fungi isolated were Peniophora sp., Xylaria sp., Polyporus dryophilus, and Polyporus adustus. 
    The increment-borer study by Hepting et al. (1949) yielded data showing that diffuse-porous wood discolored much more rapidly than ring-porous wood.  In Betula spp. and Acer spp. the discolorations were thought to be similar to those referred to as red heart and blackheart, respectively.  Nectria spp., which infected many wounds of the diffuse- porous trees, sometimes killed trees.  Although in this study Nectria spp. kept the borer holes open for 10 years in some species, no mention was made of decay.  It is possible that Nectria spp. inhibited the growth of others and thus retarded the succession of organisms leading to decay (Brandt, 1964).  Sterile growths of Poria obliqua on Betula spp. and sporophores of Fomes connatus on Acer spp. occur on Nectria cankers, suggesting that these fungi either enter the tree at the cankers, or enter at other loci and produce these growths on the cankers (W. A. Campbell and Davidson, 1938).  Only certain fungi can follow invasion by Nectria spp.

3. ORGANISMS FOLLOWING INOCULATIONS IN HARDWOODS

    Many investigators have attempted to determine the rate of growth of Hymenomycetes in living trees by placing in the tree wooden dowels supporting the growth of a known fungus (Munch, 1915; Boyce, 1920; Hirt and Eliason, 1938; Hirt, 1949a; Silverborg, 1959).  The inoculation wounds inflicted in many of these studies were similar to those made in the increment-borer studies just mentioned, and the initial processes are the same also. 
    The abrupt changes brought about by drilling may stimulate the growth of organisms already in the tree.  These organisms may greatly restrict the invasion path of inoculated organisms.  Unpublished results of the reviewer show that tissue discolorations are the first changes to follow inoculation.  From such tissues bacteria (Pseudomonas spp.) and

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nonhymenomycetous fungi-especially Phialophora spp. and Trichocladium canadense-have been isolated.  Even when the decay fungi introduced into the trees were those regarded to be aggressive in nature (such as Fomes igniarius and Polyporus glomeratus), other organisms preceded their growth, indicating a succession beginning with bacteria and non-Hymenomycetes.

4. FIRE WOUNDS AS INFECTION COURTS

Several good accounts of successions are available for hardwoods wounded by fire (Hepting, 1935, 1941; Toole, 1959). "Perhaps the most important single factor contributing to the great variation in butt-cull volume among trees of the same species and with wounds of approximately the same size and age is the fungus succession in the wood behind the wounds" (Hepting, 1941).  
    Toole (1959) listed Stereum complicatum and Schizophyllum commune as the first fungi to fruit on fire wounds.  Hepting (1941) noted that S. commune, Panus stipticus, Daldinia concentrica, Nummularia sp. (Hypoxylon sp.), Stereum sp., and Polyporus spp. fruit on the surfaces of fire wounds on oaks one year after the fire.  The second year, P. versicolor, P. pargamenus, Stereum rameale, S. lobatum, and Lenzites betulina were the most common species; and by the third year P. gilvus was present. These fungi then were followed by heart-rotters.  Results of isolations from decay behind wounds showed that the amount of decay varied greatly with the fungi causing the decay.  Stereum frustulosum and Hydnum erinaceus were isolated most frequently.  No mention of non-hymenomycetous fungi and bacteria was made in these studies, but earlier Hepting (1935) had mentioned that bacteria, Trichoderma spp., Torula spp., and Penicillium spp. were associated with some of the decay fungi.        
    Hepting (1935) pointed out that Polyporus lucidus and Lentinus tigrinus could attack old living sapwood, dead sapwood, and heartwood of the hardwoods growing on the Mississippi Delta.  Polyporus pargamenus and Stereum rameale invaded the heartwood for some distance after decaying the exposed sapwood.  Polyporus dryophilus was not able to decay the old or dead sapwood and did not induce much decay. 
    An observation of extreme importance made by Hepting (1935) in these studies concerns the pattern of decay in the trees:

    A characteristic of decay in young Delta hardwoods that is particularly striking in red gum is that decay which sets in subsequent to fire-scarring practically confines itself to the cylinder of wood extant at the time of scarring.  For example, if a gum tree is 5 inches in diameter at the time it is scarred, and composed entirely of sap-

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wood, the decay which follows will remain confined to the 5-inch cylinder, not spreading appreciably into the sapwood layers laid down after scarring.  There is, therefore, some marked difference between the sapwood extant at the time of scarring and the sapwood laid down later as to its susceptibility to decay.  This difference may possibly be due to differences in the water content of the newer and older sapwood.  This explanation is strengthened by the fact that the condition just described is most striking in red gum, which has a high water content when green; and least striking in ash, which when green has a lower water content than any other of the bottom-land species.  In ash the decay will work out further into the newer sapwood than in any of the other species studied.  The resistance of trees to the radial spread of decay is of importance in the prevention of weakening at the butt and subsequent breaking over.

    Additional investigations on the protective zone were conducted by Hepting and Blaisdell (1936). Gum-filled cells were important factors affecting invasion.  Similar observations have been made for other hard-woods (Shigo, 1965b).  An example of this in conifers seems to be shown in figures (especially Fig. 9) by Nordin (1958).

5. ORGANISMS FOLLOWING WOUNDS MADE BY ANIMALS

The yellow-bellied sapsucker, Sphyrapicus varius varius, is a pest on many tree species in Canada and the United States.  The birds drill holes in the trees and drink the sap.  Many different organisms colonize these wounds: Verticillium sp., Ceratocystis spp., Graphium sp., and Daldinia concentrica (Shigo, 1963a).  Wounds made by the red-breasted sapsucker, Sphyrapicus varius ruber, in western Canada and the United States are infection courts for Didymosphaeria oregonensis, a cause of serious cankers on Tsuga heterophylla (Ziller and Stirling, 1961).  These pioneer fungi often are followed by decay fungi.  The wood is weakened greatly where the birds concentrate their attack, and the injured growth rings sometimes separate to form ring shakes (Shigo, 1963a). Other fungi frequently grow well in these shakes. 
    Other animals are attracted to sapsucker wounds.  These include paper wasps, ruby-throated hummingbirds, woodpeckers, warblers, chipmunks, and squirrels (Kilham, 1964).  These organisms often enlarge the wounds and probably introduce microorganisms. 
    In early spring in the northeastern United States, red squirrels, Tamiasciurus hundsonicus, often bite the bark of young maple trees (Acer saccharum and A. rubrum) and drink the sap (Shigo, 1964b).  The wounds are infection courts for many organisms. Filamentous yeasts and bacteria are the predominating pioneer organisms.  The following fungi were isolated from discolored tissues extending more than 6 inches above

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and below the wounds: Verticillium sp., Cephalosporium sp., Cladosporium sp., Phialophora sp., Hypoxylon sp., and Alternaria sp.

1. RED HEART

The term "red heart" is applied to the central reddish-brown discolored tissues in Betula papyrifera, which are water-soaked in freshly cut material (W. A. Campbell and Davidson, 1941).  A similar condition is found in B. alleghaniensis and in B. platyphylla (Chao and Ts'ai, 1958).  A disease of Betula spp. in Finland called "Wisa" disease, or lilywood, appears similar; but no organisms have been associated with the discolored tissues (T. J. Hintikka, 1922). 
    Slow-growing bacteria and fungi have been isolated frequently from water-soaked tissues.  The bacterium isolated from Betula papyrifera was not identified (W. A. Campbell and Davidson, 1941), but in B. Platyphylla the major isolate was a Pseudomonas species (Chao and Ts'ai, 1958).  Torula ligniperda was consistently isolated from these water- soaked tissues and was intimately associated with the bacteria. This fungus was considered the cause of red heart by Fritz (1931), who inoculated sterile wood blocks and obtained a discoloration similar to that found in standing trees.  The red heart tissues in standing birch trees have been called-and still are called-heartwood  (Dana, 1909; also see Section IV,B).
    This erroneous conclusion is due to a lack of understanding of the processes culminating in the development of discoloration in living birch trees.  Certain discolorations develop in the absence of organisms after wounds are inflicted.  When tissues discolored in this way are invaded by organisms such as bacteria and T. ligniperda, the discoloration processes are aggravated, and red heart develops (W. A. Campbell and Davidson, 1941; Shigo, 1965b).  Red heart differs from those discolorations formed solely as a result of abiotic factors in another way; red heart tissues have a very high pH-often as high as 8.5-and the wood has a foul odor when freshly cut (W. A. Campbell and Davidson, 1941; Shigo, 1966).  
    Torula ligniperda was recognized early as a pioneer invader of wood.  It infects both conifers and hardwoods.  Von Schrenk (1900) isolated it, along with others, from "pecky" cypress.  He called the fungus Xenodochus ligniperda.  Willkomm (1866) observed the fungus in many species of trees and believed it was responsible for a red rot.  The fungus is now called Trichocladium canadense (Hughes, 1959).

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    A good account of decay following red heart is given by W. A. Campbell and Davidson (1941).  They state that decay usually had much red heart associated with it, both radially around the decayed areas and longitudinally in advance of incipient decay.  Their studies showed that once red heart developed it could persist throughout the life of the tree.  Decay fungi invaded and grew through the red heart zones.  This represents an excellent example of a succession of organisms in a living tree. 
    Dark-colored, water-soaked tissues occur in other species and are similar in many ways to red heart.  In Acer spp., blackheart-although differing in color from red heart-contains similar associated organisms, including slow-growing bacteria and Trichocladium canadense (Shigo 1965a).  An important group of fungi isolated from these discolored tissues consist of Phialophora spp. (van Beyma, 1943; Shigo, 1965b).  In many respects successions in Acer spp. are similar to those in Betula spp. (Shigo, 1965a).

2. BACTERIA AND WETWOOD

    Ever since the beginning of forest pathology the Hymenomycetes have received most of the attention.  Nonhymenomycetous fungi, and bacteria, although mentioned in some early reports, only recently have received attention.  Too often, these organisms were regarded as contaminants, and perhaps isolations were made but not mentioned for fear of inviting accusations of poor techniques.  These "other organisms," especially bacteria, are frequently associated with decay processes and can be ignored no longer. 
    The antagonistic nature of bacteria is well established (Waksman, 1947), and their ability to compete successfully under a variety of conditions gives them a distinct advantage over other organisms.  Bacteria can cause diseases of many woody plants (Cartel:, 1945; Dowson, 1957; Hartley et al., 1961). 
    Wetwood of pine and spruce has been known for many years in Sweden (Lagerberg, 1935).  The early history of the disease is given by Lagerberg (1935).  He stated that as long as the wetwood was firm, non-decay fungi and bacteria, but no rot fungi, were present.  Fungi that were normally dark had hyaline mycelium when they grew in the wet tissues.  When cracks formed and more air entered the wood, the hyphae became blue-black and the wood was termed dark wetwood.  These changes were thought to make root wetwood accessible to decay fungi.  Coniophora fusispora  was considered the principal fungus infecting dark wetwood. 
    Most studies on wetwood have dealt with species of Populus and

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Ulmus, and conifers.  From wetwood in Ulmus spp. Carter (1945) isolated four fungi in association with Erwinia nimipressuralis: Verticillium alboatrum, Dothiorella ulmi, Coniothyrium sp., and Alternaria sp.  In culture, there was a slight inhibition between V. alboatrum and Dothiorella sp. and E. nimipressuralis.  The other two fungi grew well with the bacterium. All four of these fungi followed E. nimipressuralis in the tree.    
    Clausen and Kaufert (1952) concluded from studies on Populus spp. that bacteria were present and active in heartwood and probably caused discolorations.  Reduction in compression, toughness strength, and specific gravity accompanied the discoloration.  Clausen and Kaufert (1952) mentioned non-decay fungi, and Good and J. I. Nelson (1962) showed that many non-decay fungi were associated with discolorations in aspen.  Roth ( 1950) discounted bacteria as agents affecting discoloration in Populus tulipifera. 
    Hartley et al. (1961), in a comprehensive account of wetwood and bacteria, discussed the association of wetwood and heartrot; and discolored, water-soaked wood surrounding decay has been described by many investigators.  The discolored tissues are slightly alkaline, often having a pH as high as 7 or 8.  This is too high for most wood-decay fungi.  Yet Poria obliqua grows well at such a high pH (Manka and Stube, 1952).  This may explain in part why P. obliqua forms cankers on trees as it continually infects newly formed tissues.  The fungus is not confined by the pH barrier formed by bacteria.

V. Successions of Organisms in Discoloration and Decay Processes in Living Trees, Especially Conifers

.A. Successions Involving Stereum sanguinolentum

    Most of our knowledge about successions in conifers pertains to Abies balsamea and Stereum sanguinolentum (Ekbom, 1928; Kaufert, 1935; Basham et al., 1953; Pomerleau and Etheridge, 1961; Etheridge 1962, 1963; Etheridge and Morin, 1963; A. G. Davidson and Etheridge, 1963; Zycha and Knopf, 1963). Stereum sanguinolentum is similar to S. purpureum (Brooks and Moore, 1926) and S. chailletii (Stillwell, 1960) in that it requires for successful colonization a fresh wound not infected by other organisms.  The principal infection courts for S. sanguinolentum are recently killed branches (A. G. Davidson and Etheridge, 1963; Etheridge and Morin, 1963; Etheridge, 1963). 
    Pomerleau and Etheridge (1961) showed that Kirschsteinella thujina is one of the most common fungi in dead branches of Abies balsamea.

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The fungus was recognized in earlier studies but was not identified (Christensen and Kaufert, 1932; Kaufert, 1935; Crowell, 1940). Kaufert ( 1935) stated that tissues infected by the fungus were stained light blue, appeared somewhat drier than the surrounding wood, and often were found to surround decayed tissues.   This pattern is similar to that discussed earlier for hardwoods, in which decay was surrounded by discolored tissues that yielded non-Hymenomycetes. 
    Another fungus frequently associated with Kirschsteinella thujina in Abies balsamea is Retinocyclus abietis (Pomerleau and Etheridge, 1961).  It is found chiefly in resin-soaked tissues and in buried bark around branch bases, and it has been isolated from branch wood as early as 1 year after mortality. Pomerleau and Etheridge (1961) also reported that Stereum sanguinolentum accounted for only 2.4% of the total branch infections, whereas 60% of the top infections were caused by decay fungi, mostly S. sanguinolentum.  These results, plus those of Etheridge (1963), demonstrated that slowly dying branches are not suitable points of entry for S. sanguinolentum mainly because the non-decay fungi that quickly colonize these branches prevent the successful establishment of S. sanguinolentum.   A. G. Davidson and Etheridge (1963) reported similar results after studying 600 branches killed by suppression.   The fungi R. abietis and K. thujina were isolated frequently and were considered major factors in inhibiting the invasion of S. sanguinolentum. 
    The type of wound often determines the species of pioneer fungi, which in turn determines the nature of the succession to follow.   The season of year also may be important, because the selective nature of freshly exposed wood seems to vary with the time of year (Etheridge, 1963).

    Fames annosus causes one of the most important and oldest known root diseases of conifers.  It has a worldwide distribution and is especially important in the temperate zones. Little is known about underground infections and successions involving this fungus; but above ground F. annosus is a pioneer that requires a freshly cut stump surface for successful invasion. Many examples of competition with other fungi exist, and each represents a fragmentary account of a succession (Rishbeth, 1951; Kaarik and Rennerfelt, 1957; Rennerfelt, 1957; Yde-Andersen, 1958; Meredith, 1960; Braun, 1960; Wallis, 1961).         
    Rishbeth (1950, 1951) pointed out that although Peniophora gigantea

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replaced Fomes annosus in stumps inoculated simultaneously with both fungi, Stereum sanguinolentum and Polystictus abietinus were less likely to do so.  Stereum spp., like F. annosus, require fresh substrates, uninhabited by other organisms, for successful invasion (Brooks and Moore, 1926).  Soon after pine stump surfaces are exposed, they are invaded quickly by many fungi.  Fomes annosus can compete successfully with many of these in early stages of invasion.  It can grow along stump roots already occupied by a few fungi, such as Cylindrocarpon radicicola and some blue-stain fungi, but not along roots inhabited by numerous other organisms (Rishbeth, 1951). 
    Fomes annosus is often replaced by Trichoderma viride and to some extent by Torula ligniperda.  These fungi are followed closely by others, especially Hypholoma fasciculare, Melanospora sp., and various blue-stain fungi.  Root tissues in which replacement of one fungus by another has occurred often contain zone lines, the last-formed separating F. annosus from one or more invading fungi (Rishbeth, 1951). Rishbeth (1951) stated that zone lines may slow up successions in stumps containing F. annosus by presenting at least a temporary barrier to other fungi.  One succession proceeded at a slower rate because Hypholoma fasciculare and blue-stain fungi could not pass through the zone lines. 
    Meredith (1960) outlined three stages in the succession of organisms on stumps: the Peniophora, the Hypholoma, and the Trichoderma stages.  As the stump ages, the numbers of Phycomycetes and Fungi Imperfecti increase.  A few fungi, including Biatorella resinae and Ophionectria cylindrospora, grow on the layer of resin on the stump surface.  These fungi persist only as long as fairly fresh resin is present. 
    Braun (1960) was one of the few investigators to mention bacteria as important organisms found in stumps.  He reported that certain wounds were protected from Fomes annosus by resin flow and by bacteria and nonhymenomycetous fungi.  Bacteria were discussed by Moreau and Schaeffer (1959), and in greater detail by Y de-Andersen (1958), although in the latter case the emphasis was on Armillaria mellea rather than F. annosus.  Yde-Andersen (1958) showed that bacteria, Torula ligniperda, and A. mellea were associated closely in the root tissues. 
    Meredith (1960) compared fungal successions in pine stumps with those in stems of fallen deciduous trees as presented by Mangenot (1952).  In stumps the primary colonizers were chiefly lignin-decomposing fungi.  "Sugar fungi," as described by Burges (1939), followed in the latter stages of decomposition in both dead stems and stumps.  When certain

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soil fungi grow on woody material, however, the saprophytic "sugar fungi" appear to be the pioneer organisms, whereas the lignin-decomposing fungi follow later (Garrett, 1951).

C. Successions Involving Root Organisms Other Than Fomes annosus

    Bourchier (1961) reported that normal-appearing heartwood of living Pinus contorta may support a rather constant microflora.  Whether the tissues examined were from true heartwood or from wound-initiated discolorations is not definitely known, although he states that certain fungi used in laboratory tests were isolated more often from red-stained wood infected with Stereum pini than from apparently normal wood.  As a result of laboratory tests with steamed pine blocks inoculated simultaneously with several fungi, Bourchier concluded that infection by microfungi may have preceded that by S. pini.  Some of the fungi used in the tests were Tympanis hypopodia, Retinocyclus abietis, and Coryne sarcoides.  These results suggested that in nature a succession of fungi involving S. pini may occur. 
    An interesting account of a succession of butt-rot fungi of Pinus silvestris in Poland was given by Domanski and Dzieciotowski (1955).  Polyporus tomentosus var. circinatus, Phaeolus (Polyporus) schweinitzii, and Sparassis crispa were reported to have prepared the way for the penetration to the butt by Torula sp. and Haplographium sp.  They stated that evidence was assembled indicating that the latter fungi were capable of decaying heartwood because the discolored zone that surrounded decay extended in some trees to wood unoccupied by the decay fungi.  Their results may be interpreted in the opposite way; that is, the non- Hymenomycetes invaded first, even into clear wood, and the decay fungi followed. In hardwoods (Shigo, 1965b) the decay fungi can grow through the discolored tissues, but a zone of discolored tissues, infected by non- hymenomycetous fungi, persists between the uninfected wood and the decay.  Many accounts of discolored tissues in advance of and surrounding decay have been presented.
    A succession of organisms following wounds on Abies nordmanniana is described by Shtraukh-Valeva (1954).  Small reddish discolorations characterized by a higher moisture content were associated with wounds.  These discolorations sometimes overlapped and formed columns of central rot in stems.  Shtraukh-Valeva states that the development of this condition may depend partly on the effect of atmospheric agents (air and moisture), and also on the activity of a great number and variety of weakly parasitic fungi that find favorable conditions for their development there.  Isolation attempts from 55 specimens yielded 20 mixed cul-

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tures of fungi and bacteria, while 12 yielded bacteria alone.  Shtraukh-Valeva concluded, from the type of the specimens isolated, that the wound decays were caused by a complex of microorganisms: bacteria, Ascomycetes (mostly the conidial forms) or Fungi Imperfecti, and Basidiomycetes.  The pioneer nonhymenomycetous fungi listed were species of Fusarium, Trichoderma, Penicillium, and Graphium, and the Basidiomycetes were Schizophyllum commune and Pholiota sp. 
    Shtraukh-Valeva (1954) thought air to be an important factor affecting decay.  Thacker and Good (1952), however, did not consider the composition of air in trunks of Acer saccharum as a significant factor affecting decay.  Unfortunately, these workers did not consider Polyporus glomeratus in their studies.  This fungus causes cankers, and the infection courts remain open to the air as long as the fungus is active.  For this reason air may be an important factor affecting the action of P. glomeratus. 
    Whitney (1962) investigated Polyporus tomentosus on roots and butts of Picea glauca and pointed out that, when the attack was most extensive in the heartwood, the reddish-brown discoloration occurred 1 to 3, feet ahead of the infected sapwood and bark.  Radial invasion from the heartwood through the sapwood and bark was much slower than longitudinal invasion of the heartwood.  Although other fungi were isolated from the root zone, Whitney mentioned no other fungi associated with the reddish- brown discoloration.  In this case, the other root fungi mentioned may follow invasion by P. tomentosus.  Root-infecting fungi such as Fomes annosus and P. tomentosus may be similar to Stereum spp. in their pioneer status.    
    This type of succession would seem to oppose that occurring in boles of living trees.  Or, it may be that non-Hymenomycetes have not been studied as extensively in roots as in boles.  Many unidentified fungi were isolated from decay apparently caused by Armillaria mellea in Abies lasiocarpa (Hinds et al., 1960).  Day (1950) reported that Ascomycetes and Fungi Imperfecti were common in the heartwood of spruce stems injured by drought cracks. 
    Garrett (1951) pointed out that the saprophytic "sugar fungi," typified by the Phycomycetes, are pioneer colonizers of injured, moribund, and dead plant and animal tissues.  They are adapted ecologically for this role by having an exceptionally high growth rate, and a capacity for rapid spore germination.  A rapid flare-up on a suitable substrate, followed by a period of quiescence, is characteristic of these fungi.  Burges (1939), like Garrett (1951), stated that, after initial attack by a root parasite, successions of fungi follow. He cited Helminthosporium sp. and Fusarium

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sp. as examples of pioneer invaders.  As the succession continues, wood-destroying fungi soon become dominant (Burges, 1939).  Excretions from injured or dying roots could greatly affect the type of organisms entering as pioneers, and thus affect the nature of succession (Woods, 1960). 
    An account of a succession in Pinus banksiana roots beginning at wounds made by the root weevil, Hylobius sp., and mechanical wounds was presented by Krebill and Patton (1962).  Within a few weeks after wounding, non-decay fungi were isolated from the discolored tissues near the wounds.  Fungi isolated commonly were Leptographium sp., Trichoderma sp., Pullularia sp., Penicillium spp., and several unidentified species of Fungi Imperfecti.  Hymenomycetes were not isolated until several months later.  The pioneer Hymenomycetes isolated were Polyporus tomentosus, Poria subacida, and Odontia bicolor. 
    Earlier, Whitney (1961), working with Picea glauca, described a similar succession which started at wounds made by Hylobius sp. and at other mechanical wounds.  He, too, isolated non-Hymenomycetes from discolored tissues near fresh wounds.  As the wounds aged, Hymenomycetes were isolated.  Whitney concluded this to indicate a succession that began with non-decay fungi and ended with Hymenomycetes.   That fungi were associated with the discoloration that formed very soon after the roots were wounded indicates that organisms near roots colonize wounds more rapidly than other fungi colonize wounds above ground. The environment around roots would favor such a situation. 
    The importance of competing organisms in the successful inoculation of root fungi is known (Wallis, 1961; Wallis and Reynolds, 1962).  But the possible role of bacteria in the early invasion processes of some root-infecting fungi is not well understood. 
    Although not discussed, or even mentioned, in many papers, discoloration preceding decay, and discoloration surrounding decay, is often seen in figures in publications (for example, see Fig. 4, Wallis and Reynolds, 1965).  The discoloration is often termed "incipient decay" or referred to as some type of heartwood, and few accounts of isolations from these areas are given.

VI. Successions in Trees Weakened by Parasites

1 CHESTNUT BLIGHT AND OTHER CANKER DISEASES

The most serious forest tree disease ever known was a canker disease, the chestnut blight in the United States.  This disease all but eradicated a

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valuable forest tree, and the possibility of the American chestnut tree (Castanea dentata) ever regaining its past dominance in the forest is very slight.  Probably more publications have been printed about this disease than any other forest disease in history.  In spite of this, very little information is available about the organisms that followed the aggressive fungus pathogen, Endothia parasitica. 
    It is possible that the rapidity with which trees were killed precluded nonhymenomycetous fungi.  Yet the fungus Ceratocystis fagacearum can kill Quercus spp. just as quickly, and many nonhymenomycetous fungi follow it.  The answer may be that before 1930, when the chestnut blight spread through the forests, emphasis was given to pathogens and Hymenomycetes.  A few brief accounts of the Hymenomycetes isolated following the death. of trees is given by Baxter and Gill (1931).  They stated that those fungi common on chestnut slash were the same ones found on dead standing trees: Polystictus (Polyporus) pargamenus, and Polyporus gilvus on the smaller stems and branches, and P. hirsutus and P. cinnabarinus on the larger stems and branches.  Blight-killed sprouts were attacked chiefly by the following sapwood-inhabiting fungi: Irpex lacteus, P. gilus, P. nidulans, Poria mucida, P. ferruginosa, Panus stipticus, P. rudis, Stereum sericeum, S. rameale, S. umbrinum, S. ochraceo-flavum and Peniophora cinerea.  The principal heart-rotting fungi that followed E. parasitica were Polyporus spraguei, P. pilotae, and P. sulphureus.  Observations on sporophores formed the bases for these reports. 
    The most common cankers on hardwood trees are those incited by species of Nectria (Ashcroft, 1934; Grant and Spaulding, 1938; Uri, 1948; Mooi, 1948; Lortie, 1964).  Decay fungi are known to infect trees through large open Nectria cankers (Brandt, 1964).  Poria obliqua is an example (W. A. Campbell and Davidson, 1938).  Yet there is some evidence that Nectria infections may prevent establishment of decay fungi (Brandt, 1964; Shigo, 1966).  Cankers caused by Eutypella parasitica on Acer spp. may be similar to Nectria cankers in this respect, for when Polyporus glomeratus invaded a Eutypella canker it was walled off by tissues infected by E. parasitica (R. W. Davidson and Lorenz, 1938). 
    Nectria galligena produces a plant growth substance identified as B-indoleacetic acid (IAA) (Berducou, 1952; Lortie, 1964).  The effects of the acid on tissues in trees were studied by Berducou (1952), but its effects on other organisms are not known. 
    Nectria sp. has been reported to infect lesions caused by Venturia inaequalis, Monilia sp., and Botrytis cinerea on apple trees (Wiltshire, 1921). 
    Cankers on Populus spp.. have received much attention in Europe,

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but, as with the chestnut blight disease in the United States, little is known of associated organisms and successions.  A brief report of organisms following Valsa soridida was made by Muller-Stoll and Hartmann (1950).  They mentioned Penicillium spp., Cladosporium herbarum, Trichoderma lignorum, yeasts, and sterile mycelium associated with the wood and bark around the cankers. 
    Cankers caused by Septoria musiva on hybrid poplar clones are often invaded by species of Cytospora, Fusarium, and Phomopsis (Waterman, 1945).  These secondary fungi were thought to mask the presence of S. musiva because of their rapid growth in the wood.  This account by Waterman (1945) demonstrates the importance of understanding succession of organisms involved in a disease.  Successions may sometimes proceed so rapidly that the pioneer organisms are overlooked. 
    A canker on the London plan tree, Platanus acerifolia, is caused by Ceratocystis fimbriata (Walter et al., 1940, 1952; Walter, 1946). Walter et al. (1952) pointed out that the fungus kills the cambium and bark quickly, and that a reddish-brown to bluish-black discoloration is associated with the invasion by the fungus.  Ceratocystis fimbriata was reported to be followed closely by saprophytes and wood-rotting fungi, but no mention was made of the specific organisms. 
    Aleurodiscus amorphus was shown by Hansbrough (1934) to cause cankers on suppressed Abies spp. in the United States.  The fungus has been considered a weak parasite of fir in Europe for a long time (Saccardo, 1888), and it has been described in successions on Abies spp. Falck (1927) includes the fungus in his "chain disease," in which trees are attacked first by insects, Chermes spp., next by the sooty mold Antennaria pothyophila, and then by two bark fungi, Dasyscypha calyciformis and Aleurodiscus amorphus.  Armillaria mellea frequently followed these organisms.  In this succession of organisms, which culminated in decay, the insect injury was considered the primary agent and the other organisms as secondary by Wiedemann (1927) and Plassmann (1928). 
    Cankers on Pinus resinosa caused by Tympanis pinastri serve as entry points for other organisms.  Within a year after T. pinastri infects, the bark around the cankers cracks and the sapwood is exposed (Hansbrough, 1936).  Hansbrough (1936), in his account of the successions of organisms that followed T. pinastri, considered the damage caused by secondary organisms to be very important.  Blue-stain and other fungi and bacteria were isolated from the discolored tissues in the wood.  Most of the decay was caused by Poria versipora and Radulum spathulatum, two fungi that were growing in the same tissues invaded by the staining

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fungi.  Apparently the canker on Pinus resinosa differs greatly from some hardwood cankers, which, though open, seldom serve as entry points for decay fungi. 
    Dowson (1957) points out that Prunus spp. infected by Pseudomonas mors-prunorum form cankers that are readily infected by saprophytic fungi such as Cytospora leucostoma and Diaporthe perniciosa.  This is one of the few accounts of fungi following canker-forming bacteria.

2. BEECH BARK DISEASE

    The beech bark disease results when species of Nectria infect the bark of Fagus spp. through minute wounds made by the feeding of the beech scale Cryptococcus fagi.  This disease is a classic example of a succession of organisms.  In early accounts of the disease from Europe the insect alone was thought to be the cause.  Excellent summaries of the many studies conducted on the disease are given by Ehrlich (1934).  Thomsen et al. (1949), and Schindler (1951).  The interactions of the organisms involved are discussed by Shigo (1964a).  Although the results of some investigations suggest that the disease is initiated by abiotic factors (Zycha, 1950), the concern here is with the organisms. 
    An insect, Cryptococcus fagi, is the first organism to infest the trees.  In the United States and Canada, Nectria coccinea var. faginata and another Nectria sp. are the pathogens that follow C. fagi (Shigo, 1964a); in Denmark, Nectria galligena has been cited as the pathogen (Thomsen et al., 1949). 
    The fungus pathogens are attacked frequently by the mycoparasite Gonatorrhodiella highlei (Blyth, 1949).  This mycoparasite arrests sporulation of N. coccinea var. faginata in culture (Shigo, 1964a).  The scale insects are attacked by several predators, the most important being Chilocorus stigma.  Unfortunately, this beetle also carries the spores of N. coccinea var. faginata and Fusarium sp. (Shigo, 1964a).  
    A slime flux sometimes forms on the bark before or after the fungi attack.  The bark dies under such spots.  The true nature of these spots has not been determined, but bacteria and fungi are associated with them (Ehrlich, 1934). 
    The first organisms to invade the wood after the bark has been killed by Nectria spp. are usually species of Hypoxylon (Ehrlich, 1934; Thomsen et al., 1949; Shigo, 1964a).  Hypoxylon spp. sometimes invade the bark and wood so rapidly that they render conditions unfavorable for production of Nectria perithecia. 
    At this stage, many organisms begin to attack the weakened tree; and

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determining their sequence becomes increasingly difficult.  Bark beetles attack the dying tissues.  Thomsen et al. (1949) list as important the insects Xyloterus domesticus and Hylecoetus dermestoides.  Weakened areas of the tree are attacked by woodwasps, Tremex columba (Shigo, 1964a; Stillwell, 1964).  This insect is a vector of Daedalea unicolor, a fungus inciting an important white rot of beech .( Stillwell, 1964). 
    Soon sporophores of Hymenomycetes form on the bark, and they are early indicators of sapwood decay.  Species of Stereum are usually first, followed by Polyporus adustus, Fomes fomentarius, P. radiatus, and others (Thomsen et al., 1949).  Frequently species of Stereum and Hypoxylon fruit on the same section of bark.  These organisms are associated closely. 
    Adding to this already complex situation, another scale insect on beech has been reported (Shigo, 1962a).  The insect, identified tentatively as Xylococculus betulae, also attacks Betula papyrifera and B. alleghaniensis.  This scale will attack some beech trees that apparently resisted Cryptococcus fagi.  Wounds made by X. betulae are also infected by Nectria spp.  The roughened bark around such cankers is then infested lightly by C. fagi.  Other fungi sometimes invade these dead areas, resulting in small pockets of discoloration and decay.  The organisms that follow X. betulae cause little mortality but many defective trees (Shigo, 1964a).

    Oak wilt is caused by the fungus Ceratocystis fagacearum.  This organism can kill mature trees within a few weeks.  Many other organisms invade the dying trees (Shigo, 1958).  The principal fungi isolated from recently killed trees are Hypoxylon punctulatum, Dothiorella sp., Graphium rigidum, Gliocladium roseum, H. atropunctatum, Trichoderma lignorum, Ceratocystis pluriannulata, and Trichothecium roseum (Shigo, 1958). 
    A common control method has been to deep-girdle infected trees and leave them standing (True and Gillespie, 1956).  This method caused a significant reduction in the production of subcortical mycelial mats, the fungus tissue bearing perithecia.  Trees thus treated were invaded rapidly by Hypoxylon punctulatum.  This fungus, believed to be a major factor contributing to the reduction of mycelial mats, grew through the wood so rapidly that it disrupted conditions required for mycelial mat production (Barnett, 1957; Shigo, 1958; Roncadori, 19'62). The aggressive

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nature of other species of Hypoxylon (such as Ustulina vulgaris) has been shown in studies by Wilkins (1935, 1939, 1943).  
    Another fragmentary portion of a succession related to oak wilt concerns the biotrophic mycoparasite, Gonatobotryum fuscum.  This fungus was isolated along with a species of Graphium that invaded the mycelial mats and the wood after Ceratocystis fagacearum attacked.  Shigo (1960) showed that most species of Ceratocystis, Graphium, and Leptographium were parasitized by G. fuscum.  Parasitism was affected greatly by nutrition and environment.  In some cases in the laboratory the mycoparasite was attacked by the host, Graphium sp., a reversal of parasitism.  Mycoparasitism by G. fuscum is important because the fungi it attacks are the pioneer blue-stain fungi. 
    Sapwood of lumber cut from trees killed by Ceratocystis fagacearum is invaded rapidly by this fungus.  Soon afterward, however, many other fungi also invade, and C. fagacearum is no longer readily isolated (Englerth et al., 1956). 
    Cephalosporium diospyri incites a wilt of persimmon, Diospyros virginiana.  Trees killed by the disease are decayed rapidly by Schizophyllum commune and may begin to disintegrate within 2 years (Crandall and Baker, 1950).

C. Organisms Following Rust Diseases

    Only a few accounts of organisms following rust infections are available.  Gaumann (1950) stated that Polyporus (Fames) hartigii and Agaricus (Pholiota) adiposa commonly infect fir in Central Europe via cankers formed by Melampsorella caryophyllacearum.
    The succession of organisms in Cronartium fusiforme galls on Pinus elliottii and Pinus taeda were studied by Myren (1964).  The galls were infested first by several insects: Dioryctria amatella, Eurytoma sciromatis, and Pissodes nemorensis.  The insect galleries served as infection courts for fungi.  All the galls infested by insects yielded species of imperfect fungi; 30% yielded blue-stain fungi; and 13% yielded Hymenomycetes.

Although the literature on mistletoes is voluminous (Gill and Hawks- worth, 1961), only a few reports mentioned organisms that invade trees after mistletoe (Weir and Huber, 1918; Gill, 1935; Wright, 1942; Englerth, 1942; Foster et al., 1953, 1954; Hopping and Nordin, 1962).

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Cytospora abietis is an aggressive pioneer fungus that enters the tree through mistletoe infection sites (Gill, 1935; Wright, 1942).  Wood- destroying fungi follow C. abietis, and trees are so weakened that often windthrow results.  Wright (1942) described a succession beginning with mistletoes, especially those that cause hypertrophies on red fir branches.  The mistletoe infections become infested with bark-engraver beetles, Scolytus subscaber.  The beetle carries a fungus that kills the cambium and consequently greatly weakens the branch, rendering it highly susceptible to infection by Cytospora abietis.  Sometimes the branches are weakened by aphids, and C. abietis follows.  Ants associated with the aphids are suspected of spreading spores of C. abietis picked up from pycnidia as they tend the aphids.  Wood-destroying fungi may follow and decompose the wood further. 
    Mistletoes themselves may be attacked by hyperparasites such as Septogloeum gillii and Wallrothiella arceuthobii (Hopping and Nordin, 1962).  When weakened in this manner, mistletoes are followed readily by other organisms.  In a few cases, burls on hemlocks caused by Razoumofskya tsugensis served as infection courts for Echinodontium tinctorium (Weir and Hubert, 1918).  Englerth (1942) mentioned burls or "churns" that often result when mistletoe infections become infection courts for several Hymenomycetes.  He stated that in the absence of mistletoes Fames hartigii and F. applanatus would be of practically no importance in Tsuga heterophylla.  Uninfected branches of this tree are highly decay-resistant.  Once attacked by mistletoes, however, trees are entered readily by fungi.  Similar accounts of Hymenomycetes following mistletoes are given by Foster et al. (1953, 1954).

VII. Successions in Trees Killed by Various Agents

    Mangenot (1952) conducted extensive studies on successions.  He described many pioneer organisms, following successions over a 3- to 4- year period, and conducted laboratory experiments on the principal organisms.  Most of his observations dealt with recently killed trees.  Consequently his studies centered on pioneer fungi, most of which were non-Hymenomycetes.  Some of the pioneer species listed are Mucor sp., Penicillium spp., Fusarium lateritium, Pullularia pullulans, Hormiscium sp., Cladosporium herbarium, Paecilomyces sp., Margarinomyces spp., Acrostalagmus sp., Phialophora fastigiata, Bisporomyces chlamydosporis, Cephalosporium spp., Alternaria tenuis, and Rhinocladiella sp.  His results revealed that these fungi cannot be divorced from the processes resulting in decay.

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    In later studies, Mangenot (1954) showed that, when Basidiomycetes invaded discolored tissues previously inhabited by blue-stain fungi, the pH of the tissues was lowered to 4.4.  In contrast, the pH of wood invaded first by Basidiomycetes and later by blue-stain fungi showed an increase.  These pH changes may be important factors affecting the competition of organisms in wood.  The roles of several organisms in the deterioration of logs and branches has been pointed out by Basham (1959), Chesters (1950), and Shea ( 1960).  The importance of insects and environmental factors is stressed in these reports.  In some of the studies cited by Shea, the time when sporophores appeared was used as an indicator of the time when a fungus was involved in the successions.

    The spruce budworm, Choristoneura fumiferana, causes widespread damage of Picea spp. and Abies balsamea throughout eastern Canada and the northeastern United States.  Infested trees are weakened, and many die after repeated severe attacks.  Many organisms follow C. fumiferana and contribute to the deterioration of the wood (Basham and Belyea, 1960).  Belyea (1952) discussed ten species of insects that breed in weakened and recently killed trees.  Three insects-Pityokteines sparus, Pissodes dubius, and Tetropium cinnamopterum--confine their activities to the inner bark and wood surfaces.  The next group, which includes Trypodendron lineatum, Serropalpus substriatus, Sirex juvencus, Sirex sp., and Urocerus albicornis, penetrate the wood to a limited degree.  Two other insects, Monochamus scutellatus and M. marmorator, mine deeply into the wood and contribute more directly to deterioration than all the others.  The various wounds made by all these insects pave the way for microorganisms to attack. 
    Yeasts, ambrosia fungi, other nonhymenomycetous fungi, and bacteria are often carried to wounds by insects. Many of the ambrosia beetles are associated with specific fungi indicating a symbiotic relationship (Hartig, 1844; Verrall, 1941, 1943; Wilson, 1959; Callaham and Shifrine, 1960; Batra and Franke-Grosmann, 1961).  The fungi supply the insects with food.  In addition, their growth reduces the moisture content of the wood, thus improving conditions for the insects, especially for the developing larvae (Wright, 1935).  This was pointed out by Wright (1935) for the fungus Trichosporium symbioticum and the insect Scolytus ventralis in Abies concolor.  The growth of many such fungi in wood is accompanied by discoloration.  Species of Ophiostoma (Ceratocystis) and a yeast were

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associated with discoloration around galleries of Pityokteines sprarsus (R. W. Davidson, 1955). Many investigators have isolated similar fungi from discolored tissues associated with insect galleries in dying trees (Grosmann, 1930; Wright, 1938; Verrall, 1941; Basham, 1959).    
    Stereum chailletii and Cephalosporium sp. are two aggressive fungus pioneers of sapwood of recently killed Abies balsamea (Basham, 1959, 1960).  Another fungus, Stereum sanguinolentum, also is an important pioneer fungus, although it may not appear as soon as S. chailletii (Stillwell, 1960).  The early appearance of S. chailletii is probably due to its close association with the woodwasps Sirex and Urocerus, which can attack the trees while they are dying (Stillwell, 1960). Stereum sanguinolentum also has been reported to be associated with the woodwasp Sirex gigas (Cartwright, 1938).  This fungus has been isolated most frequently from trunks in which it persists longer than does S. chailletii.  Stereum chailletii and Cephalosporium sp. have been isolated consistently from the yellowish-red discoloration that is evident during the first year after death (Basham, 1960; Stillwell, 1964). 
    Basham (1960) reported that the discolored sapwood of Abies balsamea begins to soften markedly after a year.  Polyporus abietinus is the principal fungus isolated from dead sapwood after the first year and remains so through the next 4 to 5 years.  Armillaria mellea has been isolated from trees soon after they died.  The brown-rot fungi-Fomes pinicola, Coniophora puteana, and Trechispora brinkmanni-invade trees dead longer than 4 years. Stillwell (1964) lists eleven other fungi occasionally isolated from dead sapwood. 
    Engelhardt (1957) described a succession in Tsuga heterophylla killed by the hemlock looper, Lambdina fiscellaria, that, is similar to those just mentioned.  The hemlock looper defoliated and weakened T. heterophylla, after which other insects attacked the wood and bark of the dying trees.  Ten known fungi contributed to the deterioration of the wood.  Armillaria mellea was isolated, but only after 3 years.  However, there was evidence to show that it had been in the wood much earlier.  Polyporus abietinus, one of the first fungi to invade the sapwood, could not be isolated after 2 years.  Ganoderma applanatum, G. oregonese, and Fomes annosus, three white-rot fungi, were isolated consistently during the 3-year study.  Fomes pinicola, whose sporophores formed in abundance on standing dead trees, was considered responsible for most of the decay.  Except for Polyporus abietinus and F. pinicola, few fungi formed sporophores on the trees. 
    Stillwell (1960) studied Abies balsamea killed by insects other than

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spruce budworm and pointed out that woodwasps were responsible for introducing Stereum chailletii and S. sanguinolentum.  Of 274 isolation attempts from discolored sapwood tissues, 80 were S. chailletii, 9 were S. sanguinolentum, 3 were Corticium glactinum, and 4 were Armillaria mellea.  The remaining 178 were listed as "imperfects, contaminants, or blanks (no growth)."  It would be interesting to know which fungi were associated with S. challetii and S. sanguinolentum in these trees. 
    Vaartaja and King (1964a) pointed out that Amylostereum sp. (Stereum sensu lato) was introduced into Pinus radiata by Sirex noctilio.  As Amylostereum declined, Macrophoma sabinea and Trichoderma viride grew rapidly.  Aureobasidium pullulans was associated with Amylostereum and declined with it.  Other fungi isolated were Candida sp., Graphium spp., Hormodendrum sp., Leptographium sp., Penicillium spp., and Rhizoctonia sp.  No fungi were isolated from the very moist wood near the bases of trees heavily infested by woodwasps.  Apparently Amylostereum, which infected soon after the wasps had oviposited, did not compete successfully with other fungi that likewise were finally unable to survive in the moist tissues.  This was verified further in inoculation studies by Vaartaja and King (l964b).  Throughout this review many examples show that Stereum spp. survive only when they infect tissues free of competing organisms.  As other organisms invade, Stereum spp, decline.

    Basham (1957, 1958b) described successions in fire-killed Pinus strobus, P. resinosa, and P. banksiana in Ontario., Canada.  Sapwood-staining fungi, belonging to the Fungi Imperfecti, were the first organisms to invade.  Many invaded through beetle holes.  These fungi were limited to sapwood and were abundant 1 to 3 years after tree death.  Sapwood-rotting fungi were the next largest group to invade.  These fungi, often associated closely in the tree with sapwood-staining fungi, were overrun in culture by the sapwood-staining fungi.  Of the 17 sapwood-rotting fungi isolated, 3 were responsible for 80% of the decay: Peniophora gigantea, Polyporus anceps, and Polyporus abietinus.  These fungi were regarded as important pioneer slash fungi by Spaulding and Hansbrough (1944).  Basham (1957, 1958b) gave two good examples of successions in the sapwood-rotting group.  Polyporus increased in abundance after 1 year on all three tree species, and Fomes subroseus became more abundant than F. pinicola on all three hosts after 2 years.  Most of the heartrot that followed was caused by F. pini.

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C. Organisms Following Windthrow

Buchanan (1940) investigated the deterioration of windthrown conifers in northwestern United States.  Decay fungi were not active the first 2 years.  His study illustrated the danger of relying on the presence of fruiting bodies to indicate the principal fungi in dead trees.  Thus, although Lenzites sepiaria and Polyporus versicolor formed sporophores readily, isolations showed that they were not the predominating fungi.  The ten fungi that produced fruiting bodies 8 years after the windthrow were responsible for only about 5% of the decay.  In Buchanan's study Fomes pinicola and F. applanatus were the principal invaders following the sapwood-rotting fungi.  Polyporus sulphureus and Fomes roseus did not cause much decay until after 15 years. 
    In windthrown white spruce, Picea glauca, the pioneer invader Stereum sanguinolentum has been followed by Fomes pinicola (Engelhardt et al., 1961).  The increasing abundance of F. pinicola with time is thought to be attributable to three factors: (1) a progressive increase in fungus activity, (2) the extension of F. pinicola to areas previously invaded by other fungi, including Stereum sanguinolentum, and (3) the proclivity of the fungus to fruit in down and dead material.  Engelhardt et al. (1961) concluded that the relative importance of a fungus in decay would be meaningful only when related to a stated interval of time since death. 
    Stillwell (1959) mentioned the abundance of nonhymenomycetous - fungi in windthrown trees but did not identify them.  In his studies of windthrown balsam fir, Stereum sanguinolentum and S. chailletii were the leading pioneer invaders associated with the reddish-brown or yellowish discoloration of incipient deterioration.  Although fruiting bodies of S. sanguinolentum were more abundant than those of S. chailletii, the wood yielded mostly S. chailletii-illustrating again the unreliability of using fruiting bodies to indicate the relative abundance of the fungi.  There were marked similarities in the successions occurring in insect- killed trees mentioned earlier and in windthrown trees.  Stillwell (1959) reported that Lenzites sepiaria was the primary fungus associated with advanced decay, and Polyporus abietinus was the second most important. 

D. Organisms Decomposing Slash and Litter

    An excellent example of a succession of fungi on slash of Pinus strobus in southern New England was given by Spaulding (1929) (Table I).  Lenzites sepiaria and Polystictus abietinus were pioneer fungi that

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continued to invade for 8 years.  Two other pioneer fungi, Peniophora gigantea and Stereum sanguinolentum, were active for only a few years.  The rapidly changing environmental conditions as the slash deteriorated greatly affected the growth of fungi.  The ability to grow well at high temperatures gave L. sepiaria a distinct advantage over the other fungi (Spaulding, 1929; Childs, 1939; Loman, 1965). 
    Spaulding and Hansbrough (1944) gave a good account of successions on hardwood and conifer slash in the northeastern United States. (Table II).  Nonhymenomycetous fungi were listed as principal pioneer fungi on some species of trees. 
    Elliott and Elliott (1920) described the succession of organisms on an oak branch over an 8-year period by recording the appearance of fruiting bodies of fungi and Mycetozoa.  The Ascomycete Bulgaria polymorpha was the first to fruit, after 2 years.  Coryne sarcoides and Stereum hirsutum appeared after 5 years, followed by Hypholoma fascicularis after 6 years.  The first slime mold, Physarum nutans, appeared after 7 years, along with the fungi Phlebia merismoides, Hypholoma fascicularis, and H. sublateritia.  After 8 years the following organism fruited: Pulteus cervinus, Phlebia merismoides, Physarum nutans, and Stemonitis fusca. 
    Good accounts of successions of fungi on forest litter have been given by Mikola and Hintikka (1956), Mikola (1956), and V. Hintikka (1964).  On forest litter, saprophytic fungi that have the ability to grow at very low temperatures often are the most aggressive pioneers.  Temperature is an important factor affecting the type of successions.

VIII. Successions in Pulpwood, Pulp Chips, and Wood Products

    Good general summaries of successions on bolts are given by Findlay (1940) for hardwoods and conifers.  As an example of a succession in hardwoods he cited the following succession in a beech bolt.  Non-decay fungi such as Bispora sp. and Lasiosphaeria sp. and the Hymenomycetes Stereum purpureum were the pioneer invaders.  These usually were followed by S. hirsutum, Polyporus adustus, Polystictus (Polyporus) versicolor,. and Trametes gibbosa.  Wood-boring beetles invaded next, followed finally by Myxomycetes. 
    Findlay (1940) gave a similar example for a succession in coniferous bolts.  First to appear are sap-staining fungi belonging to such genera as Ophiostoma (Ceratocystis ), Hormonema, and Cladosporium. These are

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ately after they were cut.  Trichocladium canadense could have been an inhabitant of the wood before it was cut and sprayed (see Section IV,B).  Stereum purpureum and Daldinia concentrica were the only decay fungi isolated.  Alternaria tenuis, Ceratocystis sp., and Melanconium bicolor were isolated frequently from bolts stacked for 3 and 5 weeks before being sprayed with T. viride.  Other tests showed that the wood-destroying fungi found most commonly in unsprayed stored bolts were not present in the sprayed bolts.  The common decay fungi did infect the unsprayed controls.  We may conclude, therefore, that T. viride prevented the invasion of the common decay fungi. 
    Ceratocystis virescens is one of the first fungi to infect the cut ends or hardwood bolts in New England (Shigo, 1962b).  As the dark circular patches of mycelium expand on the cut ends, white areas appear in their centers.  These white areas are colonies of Cephalosporium sp., Trichothecium roseum, and Gliocladium roseum growing over C. virescens.  The white fungi completely overgrows the mycelium of C. virescens on many bolts.  Ceratosystis pluriannulata and Graphium sp. also appear on the bolts later.

B. Successions in Wood Products

    Excellent reviews on discoloration in wood products are given by Scheffer and Lindgren (1940) and by Findlay (1959). W. G. Campbell ( 1952) gives a good account of the biological decomposition of wood.  Although little information is given directly concerning succession, these papers contribute much information indirectly pertinent to this subject. 
    Until 1937, when Bailey and Vestal (1937) showed that some Ascomycetes and Fungi Imperfecti could attack the secondary walls of wood cells, most studies on decay dealt solely with species of Basidiomycetes, and Ascomycetes in the Xylariaceae.  Since 1937, many studies on soft-rot organisms have been conducted (Savory, 1954; Savory and Pinion, 1958; Meier, 1955; Duncan 1960a, b; Zycha, 1964; and others). 
    Soft-rot fungi are pertinent in a discussion on successions because they are pioneer organisms whose growth alters the substrate, permitting other organisms to follow.  As a group, these fungi possess high tolerances for wood preservatives (Duncan, 1960a, b), and they grow well even under adverse conditions of very high pH and moisture and low aeration (Duncan, 1960a, 1961). 
    Soft-rot fungi attack hardwood timber more often than softwood.  In the laboratory, conditions that favored their action also favored rotting by white-rot fungi (Duncan, 1960b).

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Fungi isolated from living trees by Good and J. I. Nelson (1962) and Shigo (1965a) belong to genera known to contain soft-rotters.  Little is known about the role of these fungi in living trees, except that they are pioneers and that they are associated intimately with bacteria.

C. Growth of Organisms in Wood Containing Natural Toxic Materials or Preservatives

    The resistance to decay of many durable woods is due to materials in the wood that are toxic to organisms.  But some organisms can grow in wood even when such materials are present.  These pioneer organisms then alter the substrate or detoxify the substances and open the way for invasion by other wood-inhabiting organisms (Duncan and Deverall, 1964).  An example is Fistulina hepatica, which grows on Quercus spp. and Castanea spp. in nature.  This fungus will grow in a medium containing relatively high concentrations of tannins.  Such a medium inhibits growth of many other fungi (Cartwright and Findlay, 1950).  
    There are many reports indicating that certain fungi have a high tolerance to materials containing arsenic (Kaufert and Schmitz, 1937; Thom and Raper, 1932; Madhosingh, 1961), mercury (Fargher et al., 1930; Scheffer and Lindgren, 1932; F. L. Brown, 1953; Kiessling, 1961), methyl salicylate (Verrall, 1937), creosote (Christensen et al., 1942; Marsden, 1951, 1954), fluorides (Scheffer and Lindgren, 1932; Lindgren and Harvey, 1952), copper (Howard, 1922; Bayley and Weatherburn, 1945; Hirt, 1949b), and many others.  Fungi able to grow in wood containing these materials are truly pioneers, and they initiate successions.  Some of the more common fungi with this capacity are species of Penicillium, Trichoderma, Gliocladium, Hormodendrum, Aspergillus, and Alternaria.  Of possible significance is the fact, that these are all Fungi Imperfecti. 
    Some materials are toxic to many fungi but stimulate the growth of others.  Examples of such materials and the favored fungi include: borax, Alternaria; silicofluoride and tartar emetic, Trichoderma viride; organic mercury, Penicillium cyclopium; and urea, Trichoderma and Penicillium (Verrall, 1949).  The application of these materials may eliminate the organisms that normally would first invade untreated wood. 
    By favoring other organisms these materials may alter successions in ways that sometimes are of great economic importance to man.  In many cases there is a stalling or a detouring of the normal succession that leads eventually to decay.  The time gained before the normal succession resumes may permit a manufacturer to utilize the wood, which he might

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not otherwise be able to do.  Lindgren and Harvey (1952) pointed out that the principal decay fungi in bolts of conifers, Peniophora gigantea and Lenzites sepiaria, still appeared when bolts were sprayed with fluoride solution and Trichoderma invaded, but it took longer for them to become established.  On the other hand, Stereum sanguinolentum and Peniophora pitya invaded stored pulpwood treated with phenyl mercuric acetate following invasion by Penicillium roquefortii (Duncan and Deverall, 1964).  Natural checking and splitting of the wood in time also opens areas not protected by toxic materials (Findlay and Badcock, 1955).  
    Although the immediate benefits appear good when invasion by Trichoderma follows fluoride treatments, the long-range effects may not be beneficial (Hartley, 1958).  Trichoderma viride seems to cause many openings between cells, resulting in absorption of enormous amounts of preservative.  This action of the fungus can cause considerable difficulties, because if no preservatives are applied the invaded wood readily absorbs water and becomes highly susceptible to additional decay.  In contrast to this action by T. viride, bacterial infections of wood often decrease permeability.  These organisms may be the cause of irregular absorption of preservatives in some woods (Hartley, 1958). Hartley (1958) pointed out that interference with decay fungi by non-decay organisms is an important factor in the successful use of toxic substances as wood preservatives.  Non-decay fungi were believed responsible for arresting growth of decay fungi in laboratory experiments where conditions for decay were optimum. 
    A recent review by Duncan and Deverall (1964) covers many of the points already discussed, and presents some additional pertinent information.

IX. Conclusions

    Forest pathology was founded on decay studies.  Little has been added to the original principles of decay as outlined by Robert Hartig.  Research emphasis has been on the final stages of the decay process, and on Basidiomycetes, the fungi involved in the final stages.  Investigations of discolorations have been dominated by studies of blue-stain fungi in conifers, and especially of products.  Only recently have other fungi and bacteria been considered as important organisms in discoloration and decay processes. 
    The condition of wood when first infected greatly influences the events and organisms that follow. A block of sterilized wood in the laboratory

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may be decomposed completely by one fungus, and no succession of organisms is involved.  Although this proves that one organism can utilize all portions of a sterilized block of wood, the sterile conditions necessary for such actions are rare or nonexistent in nature-particularly in living trees.  Outside the laboratory, wood may be first infected when it is in one of many possible conditions.  It may be wood that has been recently formed by a living tree; it may be older wood of a living tree; wood in a tree weakened by parasites; wood in a tree killed suddenly by fire, insects or wind; cut timber; wood treated with preservatives; or wood in use.  In each case the substrate is different, and in each case many factors affect the countless pathways for the successions of organisms that follow. 
    Mechanical wounds and branch stubs are the most common infection courts that expose wood in living trees. The exposed tissues are affected first by environmental factors such as moisture and air; then they may be infected by pioneer organisms.  Discolorations initiated entirely by changes in atmospheric conditions can occur.  The invasion of organisms through such altered tissues may either enhance and accelerate the discoloring processes already occurring, or contribute significantly to the coloration, or both.  Bacteria and nonhymenomycetous fungi are pioneers in these discoloring processes. 
    To complete successful invasion, an organism must compete with all others on the infection court in overcoming the barriers formed by the living tree.  The wood is altered as it is invaded.  Usually wood-rotting Basidiomycetes follow bacteria and nonhymenomycetous fungi.  But some Basidiomycetes survive only if they are pioneers.  These fungi (such as Stereum spp. and Fomes annosus) compete poorly with non- hymenomycetous fungi and bacteria. 
    Successions in living trees are altered when parasites infect first.  Although canker-causing fungi sometimes are followed by nonhymenomycetous fungi and Basidiomycetes, they often create conditions that arrest the growth of secondary invaders.  
    Parasites that cause wilting and death often are followed by aggressive sapwood invaders. These organisms invade sapwood rapidly and alter its condition so that it can no longer support the growth and sporulation of the parasite. 
    Trees may be killed suddenly by fire, insects, and other agents.  Boring insects infest such trees and bring many organisms to the wood.  The blue-stain fungi are organisms associated commonly with and following, the insects.  Sapwood-decaying organisms invade rapidly and are followed by other fungi.  The non-Hymenomycetes still play an active role in the

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beginning processes of discoloration and decay.  Competition is intense among organisms inhabiting dead trees, but environmental factors, especially temperature and moisture, greatly affect the successions. 
    Some organisms can attack wood under extremely wet conditions and cause soft-rots.  Many nonhymenomycetous fungi are involved in these processes.  Some organisms have the ability to tolerate wood preservatives and survive in wood containing natural toxic materials.  These fungi alter the substrate to such an extent that other more damaging-but less tolerant-organisms can invade. 
    In nature many organisms are involved in the processes that begin with infection and end in total decomposition.  Decomposition of wood and other organic materials is vital to the continuance of life.  These processes must continue and will continue regardless of our actions.  Through an understanding of successions, the process perhaps can be regulated to suit our needs.

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REFERENCES

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