Three American Tragedies: Chestnut Blight, Butternut Canker, and Dutch Elm Disease
From: Exotic Pests of Eastern Forests, Conference Proceedings - April 8-10, 1997, Nashville, TN, Edited by: Kerry O. Britton, USDA Forest Service & TN Exotic Pest Plant Council
Abstract. Three North American tree species,
American chestnut (Castanea dentata), butternut (Juglans cinerea),
and American elm (Ulmus americana), have been devastated by exotic
fungal diseases over the last century. American chestnut was eliminated
from eastern forests as a dominant species by chestnut blight (Cryphonectria
parasitica). Butternut is presently being extirpated, as butternut canker
disease (Sirococcus clavigigenti-juglandacearum) spreads into northern
populations. Urban and forest American elm populations have been decimated
by Dutch elm disease (Ophiostoma ulmi and O. nova-ulmi). A
combination of basic and applied research has been directed toward developing
resistant trees of each species. Resistant American elms are now available
for planting in urban settings. The prospects for reintroduction of resistant
American chestnut, butternut, and American elm into eastern forests appear
to be promising.
Forest ecosystems are subjected to many biotic and abiotic stresses.
Native insects and diseases, droughts, windstorms and wildfire periodically
impact forests or specific tree species, leaving dead or weakened trees.
The effects of these stresses may be manifested locally or over a large
area, yet they do not cause species extinction. In contrast, exotic pests
can threaten the continued existence of a species (cf. United States Congress,
1993). Often host species have not evolved genetic resistance to exotic
pests, as coevolutionary processes have not occurred.
Three prominent North American tree species, American chestnut [Castanea
dentata (Marsh.) Borkh.], butternut (Juglans cinerea L.), and
American elm (Ulmus americana L.) have been severely impacted by
three exotic fungal diseases, chestnut blight [Cryphonectria parasitica
(Murr.) Barr], butternut canker (Sirococcus clavigigenti-juglandacearum
Nair, Kostichka & Kuntz), and Dutch elm disease [Ophiostoma ulmi
(Buis.) Narruf. and O. nova-ulmi). Below is a brief account of the
impacts of these diseases on their host species, examples of research approaches
for disease control, and a prognosis for the future of each species.
Exotic Pests and the American Chestnut
The American chestnut was once the dominant hardwood species in the eastern
United States. The tree was important to native Americans because it produced
large crops of nuts eaten by wildlife and humans, in contrast to the oaks,
hickories, and other trees that have replaced the chestnut (Schlarbaum 1989).
The species was used in many different ways by early European settlers,
providing food and timber, food for domesticated animals, and tannin. Prior
to the European colonization of North America, American chestnut was found
in vast stands from Maine to Florida, with the largest trees occurring in
the southern Appalachians. During the 19th century, however, introduced
fungal diseases would change the species composition of eastern North American
forests. An exotic fungal disease, Phytophthora cinnamomi Rands,
infested southern populations of American chestnut and the related Allegheny
chinkapin as early as 1824 (Crandall et al. 1945). This root rot disease,
thought to have caused mortality of chestnuts and chinkapins in low, moist
areas, constricted the natural range. This fungal disease was followed by
the more commonly known chestnut blight, which spread throughout eastern
hardwood forests at a rate of 24 miles per year. By the 1950s, virtually
all mature American chestnuts had succumbed to the disease. American chestnut
is now a minor understory component, existing as sprouts from old stumps
and root systems (Anagnostakis 1995).
There have been two primary research approaches to restore chestnuts
to the American forest: the use of hypovirulent strains and breeding.
Hypovirulence research: In 1953, European chestnut (C.
sativa) trees infected with blight were observed to be healing (Biraghi,
1953). Further investigation of this phenomenon revealed that unusual strains
of C. parasitica were associated with healing cankers (Grente and
Berthelay-Sauret 1978). The factors responsible for the healing from the
unusual or "hypovirulent" (sensu Grente) strains were found
to be transmissible to normal strains through hyphal anastomosis, and would
convert the normal strains to hypovirulent, thereby demonstrating potential
for biocontrol. Subsequently, the presence of unencapsidated double stranded
RNA (dsRNA) molecules were discovered in cytoplasm of hypovirulent strains,
and the dsRNA was confirmed to be a virus (Day et al. 1977). Using molecular
biology, Choi and Nuss (1992a,b) demonstrated that the genes of the virus
were the cause of hypovirulence.
A problem with using hypovirulent strains as biocontrol has been the
lackof vegetative compatibility with certain virulent strains. Without vegetative
compatibility, transformation does not occur, and the virulent strain will
eventually cause mortality. Another problem with hypovirulent strains is
the relatively limited mode of dispersal. The virus exists in the cytoplasm
and therefore, does not become involved in the sexual process, i.e., is
not contained in the ascospores. Ascospores are disseminated by wind, while
the virus containing conidia are not airborne, and have to rely upon animal
or water (rain) vectors for dispersal. Despite these limitations, hypovirulent
strains have been used to effect recovery from chestnut blight in certain
situations (Scibilia and Shain 1989, Anagnostakis 1990, MacDonald and Fulbright
1991, Brewer 1995).
Molecular biology has been used to address the limitations of hypovirulent
strains (Choi and Nuss 1992b). The molecular structure of the virus revealed
that there were only two genes that were responsible for causing debilitation
of the fungus. These genes were transferred to the fungal nucleus using
genetic engineering techniques, thereby allowing for subsequent integration
into virulent strains through sexual recombination. For every cross, approximately
50 percent of the progeny will have the debilitating genes. Sexual recombination
will also broaden the vegetative compatibility range of hypovirulent strains.
The effectiveness and spread of the transgenic fungus are currently being
evaluated in field conditions. The fungus has been found to survive for
two years, produce hypovirulent spores, and was effective in controlling
chestnut blight (Anagnostakis, personal communication).
Breeding research: Two strategies were pursued to breeding
a blight resistant American chestnut: breeding within the American chestnut
gene pool and hybridization with Asian chestnut species.
- Breeding with American chestnut populations: Although chestnut blight
had essentially removed mature chestnuts from eastern forests, there were
occasional surviving trees that were thought to possess some resistance.
Enzymatic studies of inner bark tissue revealed resistance differences,
albeit low, among trees (Samman and Barnett 1973, McCarroll and Thor 1985).
Cross pollinations were made among putative resistant trees, but resistance
could not be increased to an acceptable level and so the approach was abandoned
(Thor 1978, Schlarbaum, personal observation).
- Hybridization with Asian chestnuts: Resistance in Asian chestnut species,
particularly C. mollissima Bl. (Chinese chestnut) and C. crenata
Sieb. & Zucc. (Japanese chestnut) was evident to scientists in the
early 1900's. Breeding and testing programs were initiated by state and
Early (pre-1960) breeding programs: The U.S. Department
of Agriculture and the Connecticut Agricultural Experiment Station vigorously
tried to breed blight-resistant chestnut trees between the 1930s and the
1960s. The initial hybrids generated by these programs were not as blight
resistant as the oriental chestnut parent. To increase resistance, a breeding
strategy was adopted that crossed the first hybrids back to a resistant
parent, either a Chinese or Japanese chestnut. Unfortunately, this strategy
produced trees more similar to oriental chestnut phenotypes, e.g., short
and branching, which were not competitive in eastern forests (Schlarbaum
et al. 1994).
Despite the failure to produce a blight resistant American chestnut,
the early breeding programs left an extremely valuable legacy of knowledge
and germplasm. Methods were developed for testing trees for blight resistance.
Hybrids generated in the later phase of these programs gave the first indication
that blight resistance is partially dominant and controlled by only two
genes. Additionally, the genetic material accumulated and developed by the
old breeding programs has proved to be valuable to current breeding efforts.
These materials include: two partially blight-resistant first backcrosses
(BC1), the "Graves" tree, and the "Clapper" tree, first
generation hybrids, and pure Chinese chestnut.
Backcross Breeding Strategy: A number of breeding programs
are breeding blight-resistant American chestnut trees using the backcross
method (Burnham et al. 1986, Burnham 1990). This breeding strategy will
transfer blight resistance from Chinese chestnut to American chestnut, while
retaining the desirable growth, form, and adaptability of the American chestnut.
Highly blight-resistant progeny were recovered after intercrossing first
hybrids between Chinese and American chestnut or intercrossing first backcrosses.
There is now evidence that only a few genes control blight resistance
in Chinese chestnut, specifically, two or three incompletely dominant genes.
The evidence was provided by a combination of crossing and molecular biology.
In addition, the use of molecular techniques to accelerate the breeding
process is now considered to be feasible. A genetic map of chestnut with
regions associated with blight resistance identified, could be used to screen
newly germinated nuts for blight resistance. This may enable several generations
of backcrossing to be bypassed, yet still produce trees that have proportions
of American parentage similar to those of trees bred using conventional
Blight resistant American chestnut may soon be available for general
reforestation. The American Chestnut Foundation estimates that by 2012,
nuts will be produced from the most advanced breeding lines that can be
used in reforestation.
Chestnut gall wasp another exotic pest of chestnut:
Although blight resistant chestnuts may be available in the near future,
Phytophthora cinnamomi will still effectively restrict planting to upland
sites. On these sites, chestnuts will then be challenged by yet another
exotic pest, the chestnut gall wasp (Dryocosmus kuriphilus Yasumatsu).
Infestations by this insect were first reported in 1974 (Payne et al. 1975)
and now have spread north into Tennessee and North Carolina. Chestnut gall
wasp larvae feed upon bud and flower tissue forming a characteristic gall
and producing a toxin that can kill the infested branch. Severe infestations
can cause tree mortality.
Butternut Canker Disease and Butternut
Butternut (syn. white walnut) is a highly valued hardwood species native
to eastern North American forests. The tree is closely related to black
walnut (Juglans nigra L.) and can occur on cove hardwood, dry, and
riparian sites. The wood of butternut is highly valued for carving and for
furniture, e.g., cabinets. Butternuts were often planted on farmsteads,
close to the house. Nut kernels were used in baking, and cultivars have
been selected for orchard production (Millikan and Stefan 1989). The husk
surrounding the nut was often used to dye fabrics. In the American Civil
War, the color of Confederate uniforms was created using butternut husks
as a source of dye.
Currently, many butternut populations are being devastated by an exotic
fungal disease that causes multiple branch and stem cankers. The causal
agent of butternut canker is Sirococcus clavigignenti- juglandacearum,
a mitosporic fungus belonging to the large group of Fungi Imperfecti. This
large group encompasses those fungi where only the asexual stage of reproduction
has been found and the sexual stage remains unknown. Currently, this Sirococcus
species is thought to be an introduced pathogen, due to its sudden appearance
on butternut. The disease was first observed in Iowa in 1967 (Renlund 1971),
but is believed to have spread from the southeastern coastal region. The
age of the cankers suggests that the fungus first appeared in North America
approximately 40-50 years ago (Anderson and LaMadeleine 1978).
In 1995, the Forest Service estimated that 77 percent of the butternuts
in the Southeast were dead (USDA Forest Service 1995). Surviving butternuts
are now usually found in riparian zones, and the majority of trees are heavily
infected and not reproducing. In contrast to American chestnut, butternuts
usually will not sprout after stem death. Young trees are subject to mortality,
and fungal spores can be carried on the fruit husks (Prey and Kuntz 1982).
Therefore, when a population becomes infected, that particular gene pool
has the potential to be permanently lost. The rapid decimation of butternut
populations has been considered so severe that the U. S. Fish and Wildlife
Service has listed the species as a "species of Federal concern."
In response to the devastating effects of the butternut canker, two research
and development efforts have been formed to address this problem. The USDA
Forest Service, North Central Experiment Station, initiated a cooperative
effort with northern states and northern National Forests to locate surviving
butternuts and graft putative resistant trees into clone banks to preserve
the germplasm. Cooperators are instructed on identification of butternut
canker and conservation of germplasm (Nicholls et al. 1978, Ostry et al.
1994). Research is being conducted to develop laboratory and field protocols
to screen trees for resistance, host range studies, in vitro clonal
propagation (Pijut 1993), and the role of insects in dissemination of the
fungus. A continuing series of progress reports document the research activities
of this group.
A coalition has also been formed in the southeastern United States, by
the University of Tennessee, USDA Forest Service, Southern Region and Southern
Forest Research Experiment Station, Great Smoky Mountains National Park,
Tennessee Division of Forestry, and USGS Biological Research Division. This
coalition is working to locate surviving trees or populations, characterize
sites, identify trees with putative resistance, develop screening methodology
for disease resistance, study fungal physiology, and preserve germplasm.
Progeny/gene conservation tests were established at five locations in
1994 and three additional locations in 1995. One planting was established
under infected butternut trees for increased disease pressure. This planting
will be closely monitored for disease spread and resistant genotypes or
resistant families. Seeds collected in 1996 are presently being grown at
the East Tennessee State Nursery to provide experimental material for additional
plantings and research activities.
Pathology studies have centered around developing screening methods to
identify butternut resistance. These studies include wounding and mycelial
inoculation of seedlings under different fertilization regimes, wounding
and spore inoculation of seedlings, and log inoculations to study pathogenicity.
When possible, different genetic families (open-pollinated) are used for
inoculation. Additionally, research has been conducted on physiology and
transmission of the fungus.
Currently, the lack of knowledge about the physiology and genetics of
Sirococcus clavigignenti- juglandacearum hinders the formation of
a comprehensive strategy for protecting the butternut species. The survival
of large butternut trees in localities where the majority of butternut trees
have been destroyed suggest that genetic resistance may be present. Resistance
is present in nut selections from another Juglans species. Heartnut
[Juglans sieboldii var. cordiformis (Maxim.) Rehd.], a Japanese
walnut nut selection, has shown resistance to butternut canker and could
be used in a breeding program. Using either natural resistance or resistance
in heartnut, a backcross breeding approach coupled with the development
of a methodology for disease resistance screening has the potential to restore
this important tree species to eastern forests.
Dutch Elm Disease and American Elm
American elm usually occurs in a mixture of other hardwood species, commonly
on bottomland sites with rich, well-drained loam soils. The species' distribution
is throughout eastern North American forests, extending well into the Great
Plains. The streets of North American cities were once lined with American
elms, a fast growing, stress tolerant tree, with a vase-shaped crown. Wood
from the species was used for furniture, flooring, construction, hardwood
dimension, and veneer.
Forest and urban populations of American elm have been devastated by
two strains of Dutch elm disease (DED), a non-aggressive strain (Ophiostoma
ulmi) and an aggressive strain (O. nova-ulmi). The disease entered
the country on shipments of unpeeled veneer logs from Europe. Dying American
elms were first observed in Cleveland, Ohio in 1930 (May 1930). The disease
spread through eastern forests from three infection centers (cf.
Stipes and Campana 1981) and had spread through most of country by 1977.
Dutch elm disease has proven to be the most devastating shade tree disease
in the United States (Karnosky 1977).
Some forest populations, however, still contain large American elms,
ca. 29"+ dbh. Other native elm species, such as red elm (Ulmus rubra
Muhl.), can be infected with DED, but appear to have greater resistance.
Attempts to breed resistance into American elm using other Ulmus
species generally failed. American elm is a tetraploid, while other elm
species have diploid chromosome complements (Santamour 1969), and a reproductive
barrier exists between the two ploidy levels. Fortunately, American elms
exist that are susceptible to infection, but are tolerant to the disease.
Tolerant trees are clonally propagated by rooted cuttings. Dr. A. M. Townsend,
The U. S. National Arboretum, estimates that only 1 in 100,000 American
elm trees is tolerant to Dutch elm disease (Becker 1996). Two new cultivars,
"Valley Forge" and "New Harmony," were released by the
U. S. National Arboretum in 1996 (U. S. National Arboretum, 1996). A small
number of American elm trees which have survived the two DED epidemics are
identified each year over the wide range of this species. Seeds or cuttings
from each tree subjected to an established screening protocol are selected
for tolerance to this deadly wilt disease. Ideally, different resistances
can be brought together by hybridizing widely separated elms. To this end,
pollen from the trees which survived DED epidemics is being used in controlled
crosses with DED tolerant selections.
A cooperative project between the USDA Forest Service and the U. S. National
Arboretum has been initiated to study the genetics of host resistance in
the field and at the molecular level. Four tolerant selections have been
crossed. The resulting progenies will be DNA fingerprinted and evaluated
for disease tolerance to construct a genetic map. The genetic map could
be used to guide further tree selection in breeding programs and to understand
quantitative inheritance of disease tolerance. It is estimated that at least
10 percent of the progeny trees will have DED tolerance greater than the
Although trees with good tolerance to DED have been found, very little
is known about the mechanisms of tolerance. Research has been conducted
to identify American elm defense reactions at the biochemical level using
cell suspension cultures (Gringas et al. 1997). It will be important to
recognize similarities and differences in the mechanisms of DED tolerance
in the varied selections to enable the synthesis of unique genetic combinations.
In addition, any breeding programs directed toward improving disease resistance
would benefit from a reliable tissue culture screening method. Such a technique
could be used to eliminate years of effort in the evaluation of germplasm.
The cultures will also be used to isolate defensive chemicals and identify
genes responsible for tolerance. Differences among cell cultures in toxin
tolerance and changes in gene expression shown by the amount and type of
newly synthesized proteins have been detected. Studies by USDA Forest Service
scientists are planned to investigate the impact of elm cell secretions
on the fungus and associated toxins.
Reintroduction of American Chestnut, Butternut, and American Elm
A critical question that arises in relation to reintroduction of these
species to eastern forests is whether they can reoccupy the niche they formerly
held and successfully compete and reproduce. For butternut and American
elm, there are enough existing naturally reproducing populations that detailed
studies can be made on the silvicultural requirement for successful establishment.
No such studies can be made on American chestnut on sites within the former
natural range. However, there is indirect evidence on the growth characteristics
of the species that suggest a strategy.
Blight-resistant American chestnut trees will probably have no difficulty
in reclaiming certain sites from the relatively slower growing oaks and
hickories. Species such as yellow-poplar (Liriodendron tulipifera)
and red maple (Acer rubrum) will be vigorous competitors, but the
growth rate of chestnut seedlings suggest that chestnut will be able to
compete with these seedlings (Schlarbaum, personal observation). In blight-free
regions in the midwest, chestnut seedlings have been able to usurp niches
formerly filled by oak and other northern hardwoods. Chestnut sprouts in
clear cuts provide indirect evidence of the species' growth rate potential.
American chestnut sprouts dominate the site until infected by the blight
Another significant problem is in the mechanics of generating enough
seed for widespread reforestation of these species. Seed production from
the endpoints of breeding programs usually occurs in a seed orchard, under
the auspices of a university, state, or federal tree improvement program.
Unfortunately, government-based tree improvement programs are rapidly disappearing
due to the relatively high cost and long time periods required to generate
tangible products associated with this type of research and development
program (Schlarbaum 1995). Until this trend is reversed, general reforestation
with resistant genotypes of these species will be hampered.
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