the epidemiology of forest nursery diseases
TRANSCRIPT
Ann. Rev. Phytopathol. 1985.23:83-96 Copyright © 1985 by Annual Reviews Inc. All rights reserved
THE EPIDEMIOLOGY OF FOREST
NURSERY DISEASES
W. J. Bloomberg
Canadian Forestry Service, Pacific Forest Research Centre, 506 West Burnside Road, Victoria, B. c. V8Z IM5, Canada
INTRODUCTION
Historical
The epidemiology of forest nursery diseases has been studied much less than their etiology or ecology; consequently, only a relatively small body of information pertains to it. This article therefore emphasizes conceptual principles by which forest nursery diseases can be analyzed and categorized according to epidemiological criteria. These concepts are based on data and observations by many experienced forest nursery pathologists and practitioners.
Interestingly, epidemiological aspects were given considerable attention during the first investigations of forest nursery diseases. Although they lacked modem epidemiological methods, early nursery pathologists correctly used quantitative measures of disease increase in time and space to interpret disease mechanisms and classify types of diseases (17, 35, 37). Recently, the value of epidemiological analyses of nursery diseases is being recognized again as a result of advances in crop epidemiology generally.
Forest Nursery Versus Agricultural Crops
Although forest nursery practices have much more in common with agricultural' than with forestry operations, major differences distinguish the epidemiology of nursery diseases from that of most agricultural crops.
1. Whereas many field crops are cultivated in environments similar to those of their wild ancestors, the environments of forest nurseries are vastly different from those found under most natural forest conditions. With such great differences prevailing between the environments in which they evolved and
83
0066-4286/85/0901-0083$02.00
Ann
u. R
ev. P
hyto
path
ol. 1
985.
23:8
3-96
. Dow
nloa
ded
from
ww
w.a
nnua
lrev
iew
s.or
gby
Uni
vers
ity o
f W
aika
to o
n 07
/11/
14. F
or p
erso
nal u
se o
nly.
84 BLOOMBERG
those in which they are cultivated, nursery crops are subject to stresses that can play a strong role in inducing disease.
2. Forest nurseries are generally dispersed throughout a region rather than adjacent to one another as are farms. This spatial distribution, detennined mainly by logistic considerations, has important implications for conditions governing the spread of disease among nurseries. As a result of their locations, forest nurseries are usually surrounded by either forests or agricultural crops that may provide sources of infection or conditions suitable for disease intensification.
3. Forest nurseries occupy small areas in agricultural tenns but may be much more subdivided than farm fields into various tree species, stock types, and age classes. For example, the growing stock in a single nursery may comprise up to ten tree species, coniferous and broadleaved, in age classes ranging from newly emerged to three-year-old seedlings and various combinations of transplant stock types, e.g., 1·-1 (one year in seedbeds followed by one year in transplant beds), 2-1, 1-2. Susceptibility to and spread of disease may be affected by these factors.
4. There is usually much greater genetic variation in forest nurseries than in agricultural crops. Most forest seed is obtained from open-pollinated sources and reflects the range of genotypes and thus resistance to disease of the parent stands. Forest nurseries therefore differ from agricultural units in a number of important respects, and it will be helpful to bear these differences in mind in comparing the epidemiology of their respective diseases.
DISEASE FREQUENCY
Forest nurseries vary widely in their disease histories, as can be expected from their range of crop species, locations, and site factors. Nevertheless, nursery pathologists and practitioners have recognized types of disease frequencies that they may take into account when estimating crop losses or planning protective measures.
Chronic Diseases
Chronic diseases are characterized by their persistence from year to year or from rotation to rotation. Often they do not to respond well to control treatments successful in other tree species or nurseries. The severity of these diseases is usually sufficient to cause serious economic loss and has resulted in the abandonment of some nurseries. Examples of chronic diseases are Fusarium root rot (Fusarium oxysporum Schlecht.) in eastern and western North American nurseries (5, 26, 49), black root rot (Sclerotium bataticola Taub.) (18, 20)
Ann
u. R
ev. P
hyto
path
ol. 1
985.
23:8
3-96
. Dow
nloa
ded
from
ww
w.a
nnua
lrev
iew
s.or
gby
Uni
vers
ity o
f W
aika
to o
n 07
/11/
14. F
or p
erso
nal u
se o
nly.
NURSERY EPIDEMIOLOGY 85
and fusiform rust (Cronartiumfusiforme Hedgc. & Hunt ex Cumm.) in southern pine nurseries (11), and Phomopsis blight of junipers (Phomopsis juniperova Hahn) in nurseries of the Great Plains (33).
Chronic diseases may occur from the very start-up of a nursery, indicating serious site-related problems, or may appear after a number of disease-free years as a result of nursery practices or the introduction of pathogens from other nurseries. Black root rot losses were severe from the first year of production in a nursery established on newly cleared forest land, whereas the disease did not appear for several years in nurseries occupying former farm land (20). Evidently, abundant inoculum was already available in the forest soil but required a number of years to accumulate under successive pine seedling crops on agricultural soil. By contrast, Phytophthora root rot (Phytophthora spp.) was more prevalent in nurseries on old agricultural fields than in those on forest soils (16). Previous crops had been hosts of the pathogen and probably were sources of inoculum.
A build-up period prior to outbreaks is characteristic of some chronic diseases following the establishment of a new nursery or the introduction of a new tree species. Keithia disease of western red cedar [Didymascella thujina (Durand) Maire] in Britain becomes severe after four or five years of cropping the host species (13). This build-up is prevented by periodically removing all western red cedar from a given nursery. In some British Columbia nurseries, Fusarium root rot became severe when rotation of other species with Douglas fir was suspended in order to increase production of the latter (W. J. Bloomberg, unpublished data). Restoration of rotation schedules reduced the severity of the disease.
The outbreaks of Cylindrocladium root disease (Cylindrocladium scoparium Morgan) in Minnesota and Wisconsin nurseries (1, 44) and Phytophthora root rot in the Pacific Northwest (16) indicated that the diseases were introduced on infected stock and then had intensified because of nursery practices. Intemursery exchanges of stock are often the cause of initial introductions of chronic diseases.
Losses from chronic diseases are probably the most predictable of all types of diseases. Although they may vary from year to year, the average of several years often can be used to reliably estimate losses.
Endemic Diseases
Endemic diseases usually persist at very low intensities and ordinarily are not economically important. However, as noted below, they can flare up temporarily in serious epidemics. In some nurseries, diseases that are chronic elsewhere may be confined to endemic levels by some natural controlling factor, e.g. soil microbial populations (5).
Ann
u. R
ev. P
hyto
path
ol. 1
985.
23:8
3-96
. Dow
nloa
ded
from
ww
w.a
nnua
lrev
iew
s.or
gby
Uni
vers
ity o
f W
aika
to o
n 07
/11/
14. F
or p
erso
nal u
se o
nly.
86 BLOOMBERG
Fluctuating Diseases
Fluctuating diseases are those in which periods of one or more years of severe infection are interspersed with periods of relatively little infection. They indicate either the recurrence of conditions suitable for turning endemic diseases into epidemics or a fluctuating infection source from outside a nursery. If cyclical factors such as certain weather conditions can be recognized, it may be possible to predict losses or take protective measures. The most serious effect of fluctuating losses is disruption of outplanting programs, which may have been planned several years into the future.
Damping-off, primarily caused by Pythium spp., Fusarium spp. andRhizoc
tonia, may fluctuate greatly from year to year, depending on temperature and soil moisture conditions during germination and early seedling growth (17, 35, 37, 45). The severity of snow blight (Phacidium sp., Lophophacidium sp., Sarcotrichila sp., Hemiphacidium sp.) varies greatly according to the duration of snow cover on nursery beds (32). Fluctuation in the spore load from diseased trees within a nursery or in surrounding forests also contributes to cycles in nursery diseases. Damage in nurseries by Lophodermium needle cast [Lophodermium pinastri (Schrad.) Chev.] is to a large extent dependent on the presence of infected windbreak trees or adjacent pine stands (27, 30). Variation in spore load may also combine with variation in infection conditions to produce wide fluctuations in disease severity over time (25). Variation in spore loads from alternate plant hosts surrounding nurseries and requirements for critical infection conditions can also result in fluctuation in seedling infections, as in the case of stem rusts of jack pine (Cronartium sp., Peridermium sp.) (28) or needle rust of Douglas fir (Melampsora medusae Thurn.) and its alternate poplar hosts (21).
Sporadic Diseases Sporadic diseases have no recognizable frequency but tend to occur in
frequently. They may result from freakish combinations of factors, such as unusual weather conditions, but they also may be triggered by blunders in nursery practices, such as incorrect calibration of fertilizer or herbicide machinery, thereby rendering seedlings susceptible to otherwise weak pathogens. Since such occurrences are unpredictable, no allowance can be made for their effects on seedling production.
In many nurseries, gray mold [Botrytis cinerea (Fr.) Pers.] occurs sporadically because of the infrequent ocurrence of conditions that favor it, i.e. early frost damage, which provides infection COUlts for this weak pathogen, followed by high humidity, which favors its build-up on healthy tissues (14, 31). Overapplication of nitrogenous fertilizers combined with overly dense seeding of beds also creates conditions favorable for this disease. Correction of the predisposing conditions usually controls the disease. Other examples of sporad-
Ann
u. R
ev. P
hyto
path
ol. 1
985.
23:8
3-96
. Dow
nloa
ded
from
ww
w.a
nnua
lrev
iew
s.or
gby
Uni
vers
ity o
f W
aika
to o
n 07
/11/
14. F
or p
erso
nal u
se o
nly.
NURSERY EPIDEMIOLOGY 87
ic diseases are Rosellinia blight (Rosellinia herpotrichioides Hepting & Davidson) in Pacific Northwest nurseries (39) and Fusarium top blight in British Columbia.
Combinations of Frequency Types
Some episodes of forest nursery disease fail to conform to any one of the simplified frequency types described above. A fluctuating disease with a longer-than-average cycle may appear to be chronic if observed over a short time scale. A disease that has been sporadic in the past may become chronic if some change in nursery practice coincides with its next occurrence and so helps to perpetuate it. For example, gray mold can become chronic in container nurseries due to high seedling density or very favorable nutrient regimes (42). Chronic diseases that have been mitigated by partially successful controls in some years may exhibit a fluctuating trend; however, the underlying factors still remain. Variable success in controlling damping-off in spite of repeated applications of chemical agents may indicate the selection of tolerant strains of pathogens or a disturbance to the biological equilibrium in the soil (10).
Because of the mixture of tree species, age classes, and stock types that frequently occur in a single nursery, examples of several disease frequency types may be found concurrently, thus complicating control operations.
DISEASE PARAMETERS
Besides exhibiting different frequencies, forest nursery diseases vary with respect to growth stage of the host attacked, infection rate, symptom development, and spatial distribution. Each of these epidemiological parameters has implications for the prediction of losses and opportunities for disease management or control activities.
Host Stages
Some nursery diseases are fairly specific in the host growth stage attacked, ranging from germination through emergence to one-year and two-year-old seedlings. Other diseases may occur over more than one stage. The specificity of infection at different growth stages can sometimes be explained by interactions of host, pathogen, and environment.
Susceptible host growth stages for damping-off diseases were recognized by Hartley (17) and confirmed by others (4,37, 40), for example: germination loss or pre-emergence damping-off caused by infection of the germinating seedling radicle; normal or post-emergence damping-off caused by infection of the hypocotyl at the soil surface and generally confined to the cotyledonary stage; late damping-off caused by infection of cortical tissues in roots in the post-
Ann
u. R
ev. P
hyto
path
ol. 1
985.
23:8
3-96
. Dow
nloa
ded
from
ww
w.a
nnua
lrev
iew
s.or
gby
Uni
vers
ity o
f W
aika
to o
n 07
/11/
14. F
or p
erso
nal u
se o
nly.
88 BLOOMBERG
cotyledonary stage of growth; and top damping-off or top blight, also in the post-cotyledonary growth stage. Suggested explanations for the specificity include: (a) anatomical development of seedling tissues with age, resulting in differential resistance to soil pathogens (19); (b) strains or races of pathogens each capable of infecting seedlings at specific ages (7, 9, 15, 24); or (c) different species of pathogens becoming active as soil conditions change seasonally (9, 10, 35, 37).
In contrast to damping-off, some root rots, e.g. black root rot of pine, infect seedlings throughout the first summer of growth, becoming more severe as temperatures increase and declining in the fall. Proliferation of new roots then enables seedlings to survive when transplanted (20). Other root rots, e.g. Phytophthora root rot and Cylindrocladium root rot, cause more severe losses in transplants than in seedlings because their root systems are pruned and thus made more susceptible to infection (16,44). In some needle diseases, e.g. leaf cast oflarch (M eria laricis Vuill.), two-year-old stock is more heavily damaged than younger or older seedlings (34).
Disease Progress Rates
There are only a few records of disease progress rates in nurseries. For this reason, it is difficult to apply quantitative criteria to nursery diseases. From the available evidence, it is obvious that disease progress rates in forest nurseries may vary greatly among pathogen species, tree species, or provenances within species, and especially from year to year. In general, progress rates can be classified into four broad types:
RAPID-LIMITED DURATION RATES This type of disease-progress rate is often associated with diseases specific to a host growth stage or with the occurrence of finite periods of predisposing conditions. Disease frequency curves typically show sharp increases and decreases at the start and end of outbreaks respectively (5, 35, 37). Damage is often severe within localized areas of nurseries, affecting entire nursery beds.
Post-emergence damping-off typifies rapid-limited progress rates because of the uniform susceptibility of the majority of seedlings within a relatively short stage of their development. The seed fungus Caloscypha fulgens (Persoon) Boudier rapidly spreads among ungerminated seeds, killing up to 80% at temperatures below lOoe, but abruptly ceases activity as soon as germination occurs or warmer soil temperatures prevail (38, 43).
Foliage diseases that require moist conditions for spore germination may exhibit rapid increase as long as those cond:itions prevail, then show no further increase (29). Delays in spring seeding to avoid optimum conditions for spore germination reduced Fusiform rust infection of pine by half for every two weeks of delay (11). Incomplete synchronization of pathogen with host development
Ann
u. R
ev. P
hyto
path
ol. 1
985.
23:8
3-96
. Dow
nloa
ded
from
ww
w.a
nnua
lrev
iew
s.or
gby
Uni
vers
ity o
f W
aika
to o
n 07
/11/
14. F
or p
erso
nal u
se o
nly.
NURSERY EPIDEMIOLOGY 89
may result in truncated epidemics. Fall seeding generally reduces Fusarium root rot infection compared with spring sowing because seedlings germinate at cool soil temperatures unfavorable for the fungus. By the following summer, they have developed root systems more tolerant of the disease (5, 49).
RAPID-SUSTAINED RATES Rapid-sustained progress rates are typical of aggressive pathogens that are little affected by the host growth stage and require abundant inoculum. Damage may be severe in all nursery beds containing the host species and continue unabated throughout the growing season. Disease frequency curves may approximate a normal distribution due to increasing infection rates during the growing season, followed by declining rates during winter (5). Diseases in which infection depends on root contact with immobile inoculum, e.g. Fusarium and black and charcoal [Macrophomina phaseoli (Maubl.) Ashby] root rots, usually exhibit these progress rates because root contacts increase as root systems expand. In addition, soil temperatures remain high during the growing season, favoring these types of pathogens (5, 20, 41). Under suitable spore germination conditions, the disease progress of leaf rusts in poplar nurseries also exhibit rapid sustained rates due to the build-up of uredospore populations and the infection of new foliage. Disease progress curves approximate a logistic (sigmoid) shape as leaf surfaces became saturated with infections.
SLOW-CONTINUOUS RATES This type of rate indicates a more endemic situation than do rapid rates and are probably related to small amounts of inoculum. They may also result from an otherwise aggressive disease being held in check by control measures or by nursery practices. Disease continues to develop throughout the growing season but at lower intensities and with less economic impact. Both Cylindrocladium and Phytophthora root rots showed slower progress rates in seedbeds than in transplant beds due to slower development of the pathogens in uninjured seedling root systems than in pruned transplant beds (16, 44). Fusarium root rot was also restricted to slow continuous progress rates in nurseries with relatively cool soil temperatures (5, 49).
SPORADIC RATES Sporadic spread rates are indicative of limited flaring-up of diseases and are probably associated with localized influences such as accidental fertilizer spills, accumulations of debris piles containing inoculum, or sporadic malfunctioning of irrigation systems.
Symptom Development
Symptom development means the rate at which disease effects are expressed in the crop independently of disease progress rate. For example, a disease may progress slowly over time, but once infected, seedlings exhibit a rapid develop-
Ann
u. R
ev. P
hyto
path
ol. 1
985.
23:8
3-96
. Dow
nloa
ded
from
ww
w.a
nnua
lrev
iew
s.or
gby
Uni
vers
ity o
f W
aika
to o
n 07
/11/
14. F
or p
erso
nal u
se o
nly.
90 BLOOMBERG
ment of symptoms until death. Symptom development varies greatly with the pathogen type, host species, and physiological condition of the host, e.g. stress. Symptom development has important implications for economic loss in diseases that do not cause the death of seedlings but reduce their quality and serve as inoculum sources when they are outplanted in new plantations.
As can be expected, symptom development is generally most rapid in the youngest seedlings. In early-season damping-off, seedlings appear healthy up to a few hours before they die. The seed fungus kills seeds within a few days of mycelial contact (38). Older Douglas fir seedlings do not begin to show root rot symptoms until two months after exposure to infection by F. oxysporum (4). One-year-old red pine are usually killed during the winter following infection by Scleroderris canker [Scleroderris lagerbergii (Lagerberg.) GremmenJ. In two-year-old seedlings, symptoms are not evident until the following spring and death does not occur for another year (12). Such seedlings may appear healthy enough for outplanting but can serve as infection sources in new plantations. Rates of development of black root rot vary with pine species (18). A higher percentage of infected surviving seedlings were plantable in loblolly and longleaf than in slash pine. However, the survival of the latter 24 months after outplanting was far higher than that of longleaf. This survival pattern suggests that symptoms progress more rapidly in slash pine before outplanting but less rapidly afterward.
Environmental factors also affect the rate of symptom development in some diseases. Moisture stress hastened the death of red pine infected by Cylindrocladium root rot (44), and high temperatures increased symptom severity in slash pine inoculated with Sclerotium bataticola (20). Douglas fir seedlings in poorly drained areas were killed by Phytophthora root rot, whereas seedlings in drier soil were stunted and chlorotic (16). Transplanting such trees after they were root-pruned probably served to spread the disease within and among nurseries.
Spatial Distribution
Forest nursery diseases may be classified by their distribution in space as well as in time. General types of spatial distributions are patchy, focal-point, frontal, and random. Combinations of these types are possible; for example, a disease may exhibit a random distribution within nursery beds, but infected beds may be patchy within a nursery. Patchy distribution indicates the presence of some localized conditions favorable to disease development, including host, pathogen, and environmental factors. Concentration of inoculum at sites of diseased cull piles or at poorly drained microsites or the use of diseased seedlots can produce patchy distributions. They are distinguished from focal point distributions in that they do not spread, i.e. the inoculum is immobile and spread does not occur among seedlings. Fusarium root rot can exhibit patchy distribution as a result of variation in susceptibility among seedlots (5).
Ann
u. R
ev. P
hyto
path
ol. 1
985.
23:8
3-96
. Dow
nloa
ded
from
ww
w.a
nnua
lrev
iew
s.or
gby
Uni
vers
ity o
f W
aika
to o
n 07
/11/
14. F
or p
erso
nal u
se o
nly.
NURSERY EPIDEMIOLOGY 91
Focal-point distributions arise from the spread of disease from spot sources through some dispersion mechanism. Zoospore motility as in Pythium root rot (22), mycelial spread among seedlings as in Cylindrocladium root rot (44), or spore dispersal as in Scleroderris canker (12) are dispersion mechanisms that produce expanding foci. The source for focal-point spread may be a single infected seedling that escaped detection during grading processes (12). Patterns may at first appear to be patchy after the introduction of infected soil or soil amendments into nursery beds; the subsequent expansion and coalescence of patches then occurs because the infected material contains mobile disease organisms, e.g. nematodes in the case of corky root disease of Douglas fir (8).
Frontal distribution results from the spread of disease from a line source. Spread of the seed fungus laterally from rows sown with infected seeds (38) or of Scleroderris canker from infected transplant rows produces frontal patterns. The spread of infection from nursery boundaries with forest stands may show a frontal distribution if dispersal is limited, as in the case of heavy-spored fungi. Frontal distribution may result from the movement of water in nurseries by flooding or spillage from drainage channels. The effects may include predispositioning of waterlogged roots to weak pathogens such as Cylindrocarpon (W. J. Bloomberg, unpublished data) or spread by free-swimming zoospores (16).
Random distributions result from general dispersal of a pathogen throughout a nursery but with relatively small subsequent spread. Uniform distribution of inoculum in the soil or widespread dispersion of airborne spores, combined with generally suitable conditions for infection throughout a nursery, will result in random distribution of disease. Foliage diseases dependent on infection sources outside nurseries and stem rusts typically exhibit random distributions.
DISEASE SOURCES
The role of infection sources in nursery diseases has been discussed in connection with other epidemiological parameters. The topic is summarized below.
In general, forest nurseries are subjected to a greater variety of sources of infection than are agricultural field crops. Nurseries sited within forested areas may be invaded by the inoculum of diseases that are endemic in surrounding stands but can become epidemic under nursery conditions. Even in agricultural areas, the presence of shelterbelt trees may provide sufficient inoculum to initiate epidemics in adjacent nurseries. Within nurseries, the variety of age classes and stock types may result in infection passing from older to younger seedlings or transplants. Debris from operations such as lifting or root pruning may provide inoculum for the infection of adjacent nursery beds or succeeding crops.
Because of the variety of concurrent operations in forest nurseries, there are
Ann
u. R
ev. P
hyto
path
ol. 1
985.
23:8
3-96
. Dow
nloa
ded
from
ww
w.a
nnua
lrev
iew
s.or
gby
Uni
vers
ity o
f W
aika
to o
n 07
/11/
14. F
or p
erso
nal u
se o
nly.
92 BLOOMBERG
many opportunities for the spread of infection by the movement of machinery and labor force. Forest nurseries sited in non-forest areas often require the addition of large quantities of soil-amending matter procured from raw natural sources such as forest litter or peat bogs. These materials are sometimes sources of infection. Seed supply for forest crops is generally subjected to only superficial screening for disease, which may provide the source of seedling infection.
Airborne Disease Sources
Airborne infection sources in forest nurseries are spores from the same species or genera of trees as the seedlings, situated near nursery boundaries or as shelterbelt trees within nurseries. Lophodermium needle cast, larch needle cast, and western gall rust are examples of such airborne diseases.
Another class of airborne infection sources are the alternate plant hosts for stem rusts of pines. Airborne inoculum may also spread into nurseries in windborne dust, resulting in the re-infection of fumigated seedbeds by soil pathogens (46).
Seedborne Disease Sources
Infected seed may be responsible for introdu<:ing diseases into forest nurseries. The seed may become infected prior to being collected, as a result of storage and processing, or a combination of both (43).
Soilborne Disease Sources
Soilborne infection sources may be indigenous to the sites on which nurseries have been established or they may be introduced as a result of transplanting infected stock from other nurseries, importing infected soil or soil amendments, or using infected seed.
Waterborne Disease Sources
Waterborne diseases may be introduced into nurseries through irrigation systems and improperly located drainage arrangements. Waterborne sources are especially important in diseases spread by free-swimming zoospores.
Organic-Residue Disease Sources
Organic-residue infection sources include peat, leaf litter, sawdust, and other types of soil amendments intended to increase the organic-matter content of forest nursery soils. They are often infested with pathogenic soil organisms (3). Even more dangerous is the use of culled seedlings for compost material, since disease is often the reason for culling. Dead and diseased seedlings in nursery beds constitute infected residues if they are not removed during weeding or lifting operations. Overwintering and resting spores present in such material insure the continuation of disease life cycles. A number of agricultural crops
Ann
u. R
ev. P
hyto
path
ol. 1
985.
23:8
3-96
. Dow
nloa
ded
from
ww
w.a
nnua
lrev
iew
s.or
gby
Uni
vers
ity o
f W
aika
to o
n 07
/11/
14. F
or p
erso
nal u
se o
nly.
NURSERY EPIDEMIOLOGY 93
used as green manures are capable of increasing the amounts of inoculum or acting as bridging hosts between rotations (36, 47).
EPIDEMIC FACTORS
Because forest nurseries lack the moderating influences in natural forests, environmental factors play a strong role in epidemics of seedling diseases. The most important factors are moisture and temperature. Extremes of these factors may cause endemic diseases to become epidemic through stresses or direct
.
injury to seedlings or through increasing the activities of pathogens. Examples have been cited above of frost damage and excess moisture predisposing seedlings to gray mold and Cylindrocarpon root rot respectively. In poplar nurseries, weak pathogens such as Cytospora chrysosperma can cause serious economic loss in moisture-stressed coppice shoots (2).
Between damaging extremes, environmental factors may tilt the balance in favor of seedling or pathogen. Temperature and moisture conditions that hasten the germination and growth of seedlings also shorten the period of vulnerability to early damping-off, whereas prolonged cool, wet periods after seeding enhance disease (17, 35, 37,38). Warm soil temperatures during the first 30
days after seeding are more important in the development of Fusarium root rot than are high temperatures later in the growing season (5). Other root rots also require warm soils to cause serious damage. The distribution of Phytophthora root rot in nurseries appears to be governed by both soil moisture and the temperature requirements of the disease. Canadian nurseries apparently are too cool and southwestern United States nurseries too dry for serious losses to occur. Conditions in the Pacific Northwest and the east and southeastern US are more favorable to the disease.
A favorable balance of temperature and moisture is necessary for the development of nursery diseases spread by airborne spores. In stem rusts, a relatively narrow temperature range combined with a high relative humidity is required over a minimum period for infection of pine seedlings (11, 28). Moisture as rain or irrigation water is a factor in the intensification of diseases spread by waterborne spores, e.g. Sirococcus tip blight (Sirococcus strobilinus Preuss.), Scleroderris canker, brown spot needle blight [Scirrhia acicola (Deam.) Siggers] (23), and Dothistroma needle blight (Dothistroma pini Hulbary).
Other factors affecting the severity of nursery diseases include the pH, nutrient status, and structure of the soil. Early observations that damping-off is more severe in alkaline than in acid soils were interpreted as conditions favoring the pathogen, especially Pythium sp. (17, 35, 37). However, it has since been recognized that the tolerance of various host species for alkalinity in soils may be just as important. In addition, acidification through the addition of organic
Ann
u. R
ev. P
hyto
path
ol. 1
985.
23:8
3-96
. Dow
nloa
ded
from
ww
w.a
nnua
lrev
iew
s.or
gby
Uni
vers
ity o
f W
aika
to o
n 07
/11/
14. F
or p
erso
nal u
se o
nly.
94 BLOOMBERG
materials, e.g. peat, controls damping-off more effectively than chemical acidification (J. E. Bier, unpublished data), suggesting that soil structure may be a factor. Soil nutrient status, especially large amounts of nitrogen, may affect disease severity by increasing tissue succulence. Soil structure and texture also affect disease losses. Damping-off tends to be more severe in heavy clay soils, whereas black root rot and corky root are more prevalent in sandy soils (8, 20).
APPLICATION OF EPIDEMIOLOGICAL METHODS
Undoubtedly, systematic application of epidemiological methods to nursery disease research would lead to better und(:rstanding of disease processes, damage, and control. Epidemiological information usually is acquired only as an adjunct to etiological and ecological studies rather than as a means for epidemic analysis. Relatively few investigations report disease progress rates or spatial distributions; often control experiments are unsuccessful because underlying epidemiological factors are not clearly understood. Prediction of disease losses is not regularly attempted in forest nurseries because of the many unknown variables. Clearly, acquisition of II comprehensive body of data on disease frequencies and timing, amounts and sources of inoculum, various environmental factors, and stages of seedling development must be a priority objective for nursery pathologists. Such data are essential if pathologists want to progress from a crisis-oriented to a crop-health maintenance approach to nursery disease management.
Simulation modeling is a promising approach to epidemiological analysis of nursery diseases. Predictive models use disease increase measurements to define progress curves by mathematical parameters. Disease management models estimate the effects of different nursery practices on disease development. Models merely fonnalize existing epidemiological infonnation but in doing so clarify the processes involved in dislease development. For example, a model of Fusarium damping-off and root rot of Douglas fir emphasized the critical role of inoculum densities in the upper soil horizons because of the small size of seedling root systems at these soil depths early in the growing season (6). A single infection at this stage more likely led to death than did multiple infections in the lower soil horizons because: root systems penetrating to these depths were much larger and capable of sustaining the seedling. In addition, soil temperatures were lower than they were close to the surface; therefore, the pathogen progressed more slowly in the roots. Control procedures should therefore concentrate on inoculum reduction in the first few centimeters of soil.
Although a powerful technique, mathematical modeling is dependent on the availability of reliable field and laboratory data. Regardless of whether the epidemiologies of nursery diseases are elucidated by modeling or by any other
Ann
u. R
ev. P
hyto
path
ol. 1
985.
23:8
3-96
. Dow
nloa
ded
from
ww
w.a
nnua
lrev
iew
s.or
gby
Uni
vers
ity o
f W
aika
to o
n 07
/11/
14. F
or p
erso
nal u
se o
nly.
NURSERY EPIDEMIOLOGY 95
method of investigation, the acquisition of a useful body of epidemiological data on forest nursery diseases will require time and effort by nursery pathologists. It is a worthwhile objective.
Literature Cited
1. Anderson, N. A., French, D. W., Taylor, D. P. 1962. Cylindrocladium root rot of conifers in Minnesota. For. Sci. 8:378-82
2. Bloomberg, W. J. 1962. Cytospora canker of poplars: Factors influencing development of the disease. Can. 1. Bot. 40:1271-80
3. Bloomberg, W. J. 1964. Use of organic residues in forest nurseries. Dep. For. Bimon. Prog. Rep. 19(6):4
4. Bloomberg, W. J. 1971. Diseases of Douglas-fir caused by Fusarium oxysporurn. Phytopathology 61:467-70
5. Bloomberg, W. J. 1973. Fusarium root rot of Douglas-fir seedlings. Phytopathology 63:337--41
6. Bloomberg, W. J. 1979. Model simulations of infection of Douglas-fir seedlings by Fusarium oxysporum. Phytopathology 69:1072-77
7. Bloomberg, W. J., Lock, W. 1972. Strain differences in Fusarium oxysporurn causing diseases of Douglas-fir. Phytopathology 62:481-85
8. Bloomberg, W. J., Sutherland, J. R. 1971. Phenology and fungus-nematode relations of corky root disease of Douglas-fir. Ann. Appl. Bioi. 69:265-76
9. Brownell, K. H., Schneider, R. W. 1983. Fusarium hypocotyl rot of sugar pine in California forest nurseries. Plant Dis. 67:105-7
10. Buxton, E. W., Sinha, I., Ward, V. 1962. Soil-borne disease of Sitka spruce seedlings in a forest nursery. Trans. Br. Myeol. Soc. 45:433--48
11. Czabator, F. J. 1971. Fusiform rust of southern pines-A critical review. US For. Servo Res. Pap. SO-65. New Orleans, LA: US For. Servo S. Exp. Sta. 39 pp.
12. Dorworth, C. E. 1970. Scleroderris canker in Ontario forest nurseries. Can. For. Serv.lnf. Rep. O-X-14B. Sault Ste. Marie, ant.: Can. For. Serv. Gr. Lakes For. Res. Ctr. 9 pp.
13. Forestry Commission, UK. 1967. Keithia disease of western red cedar, Thuja plicata. Leajl. 43. 7 pp.
14. Halber, M. 1963. Botrytis sp. on Douglas-fir seedlings. Plant Dis. Rep. 47:556
15. Hanioja, P. 1969. Taimipoltteen aiheuttajista metsantutkimuslaitoksen Punka-
harjun Koeaseman Taimitarhoissa. Helsinki: Camm. Inst. For. Fenn. 69. 21 pp.
16. Hansen, E. M., Hamm, P. B., Julis, A. J., Roth, L. F. 1979. Isolation, incidence and management of Phytophthora in forest tree nurseries in the Pacific northwest. Plant Dis. Rep. 63:607-11
17. Hartley, C. 1921. Damping-off in forest nurseries. US Dep. Agrie. Bull. 934. Washington, DC: US Dept. Agric. 100 pp.
18. Henry, B. W. 1953. A root rot of southern pine nursery seedlings and its control by soil fumigation. Phytopathology 43:81-88
19. Hock, W. K., Klarman, W. L. 1967. The function of the cndodermis in resistance of Virginia pine seedlings to dampingoff. For. Sci. 13: 108-11
20. Hodges, C. S. 1962. Black root fOt of pine seedlings. Phytopathology 52:210-19
21. Hunt, R. S. 1978. Meiampsora foliage rusts in British Columbia. Can. For. Servo FPL 49. Victoria, BC: Can. For. Servo Pac. For. Res. Ctr. 4 pp.
22. James, R. L. 1982. Pythium root disease of Douglas-fir and grand fir seedlings at the Coeur d'Alene nursery, Idaho. US For. Servo North. Reg. Rep. 82-10. MisSOUla, MT: US For. Serv. 10 pp.
23. Kais, A. G. 1971. Dispersal of Scirrhi a acicola spores in southern Mississippi. Plant Dis. Rep. 43:309-11
24. Lang, K. J. 1976. Expcrimcnte mit erregern der umfallktankheit. II. Einzel-und mischinfektionem mit umfallerregern an Trichoderma viride Pefs. ex Fr. an koniferensamlingen verschiedener herkunft. Eur. J. For. Pathol. 6:46--56
25. Lanier, L., Sylvestre, G. 1971. Epidemiologie du Lophodermium pinastri (Schrad.) Chev. Eur. J. For. Pathol. 1:50--63
26. Merrill, W., McCall, K., Zang, L. 1981. Fusarium root rot of Douglas-fir and Fraser fir seedlings in Pennsylvania. Plant Dis. 65:913-14
27. Nicholls, T. N., Skilling, D. D. 1970. Lophodermium pinastri outbreak in Lake states forest nurseries. Plant Dis. Rep. 54:731-33
28. Nighswander, J. E., Patton, R. F. 1965. The epidemiology of the jack pine-oak
Ann
u. R
ev. P
hyto
path
ol. 1
985.
23:8
3-96
. Dow
nloa
ded
from
ww
w.a
nnua
lrev
iew
s.or
gby
Uni
vers
ity o
f W
aika
to o
n 07
/11/
14. F
or p
erso
nal u
se o
nly.
96 BLOOMBERG
gall rust (Cronartium quercuum) in Wisconsin. Can. J. Bot. 43:1561-81
29. Parker, A. K. , Long, J. R. 1961. Botrytis sp. associated with damage to Douglasfir nursery stock. Can. Dep. Agric. Sci. Servo BiMon. Prog. Rep. 17(2):1
30. Pawsey, R. G. 1964. Needle-cast of pine (Lophodermium pinastri). UK For. Comm. Leafl. 48. London: UK For. Comm. 7 pp.
31. Pawsey, R. G. 1964. Grey mould in forest nurseries (Botrytis cinerea). UK For. Comm. Leafl. 50. London: UK For. Comm. 7 pp.
32. Peace, T. R. 1962. Pathology of Trees and Shrubs. Oxford: Clarendon. 753 pp.
33. Peterson, G. W. 1975. Phomopsis blight of junipers. US For. Servo Agric. Handbk. 470:76-79. Washington, DC: US For. Servo
34. Phillips, D. H. 1963. Leaf cast of larch. Meria laricis. UK For. Comm. Leaf!. 21. London: UK For. Comm. 4 pp.
35. Pomerleau, R. 1942. Etudes sur la fonte des semis de conireres. Rev. Trimest. Can. 110:127-53
36. Redfern, D. B. 1970. The effect of plant residues on damping-off of Pinus resinosa seedlings. Tree PLant. Notes 21(4): 13-15
37. Roth, L. F. , Riker, A. J. 1943. Seasonal development in the nursery of dampingoff of red pine seedlings caused by Pythium and Rhizoctonia. J. Agric. Res. 67:417-31
38. Salt, G. A. 1974. Etiology and morphology of Geniculodendron pyriforme gen. et sp. nov., a pathogen of conifer seeds. Trans. Br. Mycol. Soc. 63:339-51
39. Shea, K. R. 1964. Rosellinia herpotrichioides on Sitka spruce seedlings in Washington. Plant Dis. Rep. 48:512-13
40. Shea, K. R. , Rediske, J. H. 1961. Pathological aspects of germination and sur-
vival of Douglas-fir in controlled environment. Weyerhaeuser Co. For. Res. Note. 41. Centralia, WA: Weyerhaeuser. 8 pp.
41. Smith, R. S. , Bega, R. V. 1964. Macrophomina phaseoli in the forest tree nurseries of California. PLant Dis. Rep. 48:206
42. Sutherland, J. R. , Van Eerden, E. 1980. Diseases and insect pests in British Columbia forest nurseries. Br. Columbia Min. For.lCan. For. Servo Jt. Rep. 12. Victoria, BC: Can. For. Servo 55 pp.
43. Sutherland, J. R. , Woods, T. A. D. 1978. The fungus Geniculodendron pyriforme in stored Sitka spruce seeds: Effects of seed extraction and cone collection methods on disease incidence. Phytopathology 68:747-50
44. Thies, W. G. , Patton, R. F. 1970. The biOlogy of Cylindroc1adium scoparium in Wisconsin forest tree nurseries. Phytopathology 60:1662-68
45. Tint, H. 1945. Studies in the Fusarium damping-off of conifers. III. Relation of temperature and sunlight to the pathogenicity of Fusarium. Phytopathology 35:498-510
46. Vaartaja, 0.1964. Survival of Fusarium, Pythium, and Rhizoctonia in very dry soil. Can. Dep. Agr. Sci. Servo BiMon. Prog. Rep. 20(2):3
47. Wall, R. E. 1984. Effects of recently incorporated organic amendments on damping-off of conifer seedlings. Plant Dis. 68:59-60
48. Warcup, J. H. 1952. Effect of partial sterilization by steam or formalin on damping-off of Sitka spruce. Trans. Br. Mycol. Soc. 35:248-62
49. Wright, E. , Harvey, G. M. , Bigelow, C. A. 1963. Tests to control Fusarium root rot of Ponderosa pine in the Pacific northwest. Tree Plant. Notes 59: 15-20
Ann
u. R
ev. P
hyto
path
ol. 1
985.
23:8
3-96
. Dow
nloa
ded
from
ww
w.a
nnua
lrev
iew
s.or
gby
Uni
vers
ity o
f W
aika
to o
n 07
/11/
14. F
or p
erso
nal u
se o
nly.
Annual Review of Phytopathology Volume 23. 1985
CONTENTS
PREFATORY CHAPTER
Plant Pathology at the Crossroads, Arthur Kelman
HISTORICAL PERSPECTIVES
William Brown: Pioneer Leader in Plant Pathology, S. D.
Garrett 13
Ernst Giiumann, 1893-1963: Pioneer Leader in Plant Pathology, H. Kern 19
ApPRAISAL OF PLANT DISEASE
The Spatial Analysis of Soilborne Pathogens and Root Diseases,
C. Lee Campbell and James P. Noe 129
Limiting the Effect of Disease Resistance on Yield, V.
Smedegaard-Petersen and K. Tolstrup 475
PATHOGENS/PUNGI
The Biology, Ecology, and Control of Sclerotium rolfsii. Z. K.
h* �
Parasite: Host: Environment Specificity in the Cereal Rusts, L. E.
Browder 201
PATHOGENS/BACTERIA
The Molecular Genetics of Plant Pathogenic Bacteria and Their
Plasmids, Nickolas J. Panopoulos and Richard C. Peet 381
PATHOGENS/NEMATODES
The Ecology of Nematodes in Agroecosystems, Diana W.
Freckman and Edward P. Caswell 275
PATHOGENS/VIRUSES
Advances in Geminivirus Research, B. D. Harrison 55
PHYSIOLOGY OF HOST-PATHOGEN INTERACTION
Transposon Mutagenesis and Its Potential for StUdying Virulence
Genes in Plant Pathogens, Dallice Mills 297
(Continued) vii
/ A
nnu.
Rev
. Phy
topa
thol
. 198
5.23
:83-
96. D
ownl
oade
d fr
om w
ww
.ann
ualr
evie
ws.
org
by U
nive
rsity
of
Wai
kato
on
07/1
1/14
. For
per
sona
l use
onl
y.
viii CONTENTS (Continued)
Enzymatic Penetration of the Plant Cuticle by Fungal Pathogens, P. E. Kolattukudy 223
BREEDING FOR RESISTANCE
Strategies in Unconventional Breeding for Disease Resistance,
Gerhard Wenzel 149
The Current Status and Prospects of Multiline Cultivars and
Variety Mixtures for Disease Resistance, M. S. Wolfe 251
EPIDEMIOLOGY AND INFLUENCE OF ENVIRONMENT
The Epidemiology of Forest Nursery Diseases, W. J. Bloomberg 83
A Comparison of Simulation Approaches to Epidemic Modeling,
P. S. Teng 351
ACTION OF TOXICANTS AND CHEMICAL CONTROL
The Bioregulatory Action of Flavor Compounds on Fungal
Spores and Other Propagules, Richard C. French 173
The Chemical Control of Post-Harvest Diseases: Subtropical and
Tropical Fruits, Joseph W. Eckert and Joseph M. Ogawa 421
BIOLOGICAL AND CULTURAL CONTROL
Trichoderma and Gliocladium: Biology, Ecology, and Potential
for Biocontrol, G. C. Papavizas 23
SPECIAL TOPICS
Monoclonal Antibodies in Plant Disease Research, Edward L.
Halk and Solke H. De Boer 321
On the Conceptual Basis of Crop Loss Assessment: The
Threshold Theory, J. C. Zadoks 455
Plant Pathology in the Small Farm Context, Raul A. Moreno 491 Ann
u. R
ev. P
hyto
path
ol. 1
985.
23:8
3-96
. Dow
nloa
ded
from
ww
w.a
nnua
lrev
iew
s.or
gby
Uni
vers
ity o
f W
aika
to o
n 07
/11/
14. F
or p
erso
nal u
se o
nly.