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New Zealand Journal of Forestry Science 33(3)
MYCOSPHAERELLA LEAF DISEASES
OF TEMPERATE EUCALYPTS
AROUND THE SOUTHERN PACIFIC RIM*
C. MOHAMMED†‡,
CSIRO Forestry and Forest Products,
Private Bag 12, Hobart, Tasmania 7001, Australia
T. WARDLAW,
Forestry Tasmania, GPO Box 207, Hobart, Tasmania 7001, Australia
A. SMITH, E. PINKARD, M. BATTAGLIA,
Co-operative Research Centre for Sustainable Production Forestry,
Private Bag 12, Hobart, Tasmania 7001, Australia
M. GLEN, I. TOMMERUP,
CSIRO Forestry and Forest Products,
Underwood Avenue, Floreat, Western Australia 6014, Australia
B. POTTS and R. VAILLANCOURT
Co-operative Research Centre for Sustainable Production Forestry,
Private Bag 12, Hobart, Tasmania 7001, Australia
(Received for publication 9 March 2004)
ABSTRACT
Research with Mycosphaerella spp. on eucalypts has been historically and
strongly focused towards taxonomical species descriptions, extension of host, and
geographical range. To date there is insufficient information to develop management
prescriptions that can be applied operationally.
The research concept we have adopted is an integration of empirical studies
(detection, impact, epidemiology, and physiology) and designed experiments that
provide a knowledge base from which models can be developed and validated. Our
empirical studies and designed experiments form a core response to current industry
priorities in Australia.
Keywords: Mycosphaerella leaf disease; disease management tools; in planta
molecular detection; process-based growth model; host resistance.
* Paper presented at the 8th International Congress of Plant Pathology, 2–7 February 2003,
Christchurch, New Zealand.
† Also: Co-operative Research Centre for Sustainable Production Forestry
‡ Corresponding author
New Zealand Journal of Forestry Science 33(3): 362–372 (2003)
Mohammed et al. — Mycosphaerella leaf diseases
363
INTRODUCTION
This paper reviews the status of Mycosphaerella leaf diseases on temperate eucalypt
species in the south Pacific Rim countries. We describe research based in Tasmania that is
being conducted using Mycosphaerella leaf disease as a case study. We aim to provide a
knowledge base, a new approach, and tools for developing viable prescriptions for disease
management in plantation eucalypts.
TAXONOMY, EPIDEMIOLOGY, AND BIOLOGY
Over 30 species of Mycosphaerella have been recorded on eucalypts (Carnegie &
Keane 1998; Crous 1998; Dick & Dobbie 2001; Milgate et al. 2001; Maxwell et al. 2003).
Commonly a suite of leaf pathogens is found together in an area although only a small
number, particularly M. nubilosa (Cooke) Hansf. and M. cryptica (Cooke) Hansf., appear
responsible for significant damage (Park et al. 2000).
Mycosphaerella leaf disease causes loss in photosynthetic area (leaf spotting, shoot
blight, and defoliation). It can lead to poor tree form and occasionally death. Damage may
be “one-off” or sustained over fairly long periods. It is often difficult to confidently
differentiate species of Mycosphaerella — especially as more than one can be present on
a leaf — based on field symptoms such as the morphology of lesions or the distribution of
fruit bodies. A more reliable characteristic is the development of germ tubes during
ascospore germination. For example, in M. cryptica, germ tubes develop from only one cell
of the ascospore, while in M. nubilosa germ tubes develop from both cells (Crous 1998).
This type of character, however, is of no value for diagnosis in the field.
The only in-depth studies of the epidemiology and biology of Mycosphaerella leaf
disease have been for M. cryptica and M. nubilosa (Cheah 1977; Beresford 1978; Ganapathi
1979; Cheah & Hartill 1987; Park & Keane 1987; Park 1988a, b; Carnegie 2000).
Ascospore germination and subsequent leaf infection for M. cryptica and M. nubilosa have
been reported by Park to be optimal under conditions of 5–7 days’ leaf wetness at 15–20°C.
Ascospore release requires the presence of free water (Beresford 1978; Cheah 1977; Park
1988a). Flushes of new growth appear more susceptible to infection and so disease
development also depends partially upon the growth cycle. Severe epidemics are often seen
in plantations with trees in juvenile foliage. Significant leaf disease, therefore, develops
only in areas that have a climate that provides sufficient periods of leaf wetness and
temperatures within the optimum range for leaf infection, lesion development, and spore
discharge which coincide with a disease-prone stage of the host.
The areas in the southern Pacific Rim where damage from Mycosphaerella spp. has
been reported to be severe are:
•
The coastal regions of Chile where severe (complete) defoliation of young E. globulus
Labill. has been observed. Surveys have identified a suite of species, including known
damaging species such as M. cryptica and M. marksii Carnegie & Keane, and seven
other species of Mycosphaerella (six new to Chile) associated with leaf disease
symptoms (Ahumada et al. 2003). Mycosphaerella nubilosa was not reported by
Ahumada.
•
The central North Island of New Zealand. Mycosphaerella problems have been
reported as serious on those eucalypt species that are no longer widely planted (e.g.,
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New Zealand Journal of Forestry Science 33(3)
E. delegatensis R.T.Baker). Mycosphaerella cryptica is the major cause of
Mycosphaerella leaf disease in New Zealand, although M. nubilosa is present (Dick
1982; Dick & Gadgil 1983). Phaeophleospora eucalypti (Cooke & Massee) Crous,
Ferreira & Sutton is the most significant leaf pathogen at the moment on the main
species currently planted (E. nitens (Deane & Maiden) Maiden) (Margaret Dick pers.
comm.).
•
South-eastern Australia, where Mycosphaerella leaf disease has been of sporadic
concern over the last three decades in the eucalypt plantation estate. In Tasmania
severe damage from M. cryptica and M. nubilosa is concentrated in E. globulus
plantations in north-west Tasmania where recent expansion of these plantations has
exacerbated the problem. Mycosphaerella tasmaniensis Crous & M.J.Wingf. (Crous
et al. 1998) is associated with severe leaf disease and shoot blight of E. nitens on cold
high-altitude sites. Historically in Victoria severe Mycosphaerella epidemics occur in
E. globulus plantations in Gippsland (Reinoso 1992; Carnegie 2000; Carnegie & Ades
2002). The incidence of Mycosphaerella is now increasing in the Green Triangle of
western Victoria (and eastern South Australia) following the rapid expansion of
E. globulus plantations during the late 1990s (Paul Barber pers. comm.).
•
South-western Australia, where the number of Mycosphaerella species associated
with Mycosphaerella leaf disease appears to have increased considerably over the past
10 years. Ten years ago studies by Abbott et al. (1993) and Carnegie et al. (1997)
reported the disease to be more severe in regrowth areas of native forests and relatively
low in plantation areas. Since Abbott’s study in 1993, the Mycosphaerella inoculum
load has increased and disease, especially that caused by M. cryptica, is now prevalent
in plantations. Not only has the number of reported species increased, but first records
and new descriptions of potentially damaging species (i.e., M. nubilosa) are frequent
(Maxwell et al. 2003).
Mycosphaerella leaf disease is not considered a major health issue in eucalypt
plantations elsewhere in Australia. In south-east New South Wales, Mycosphaerella leaf
disease causes sporadic problems in E. globulus plantations. Mycosphaerella cryptica can
be a problem on E. nitens in the higher altitude areas of New South Wales but is not
widespread. Eucalyptus pilularis Smith is the host most susceptible to Mycosphaerella spp.
in northern New South Wales (Angus Carnegie pers. comm.). In Queensland, the subtropical hardwood plantation estate is relatively small and in a state of expansion. The
immediate and most evident damaging disease agent is the foliar pathogen Quambalaria
pitereka (J.Walker & Bertus) J.A.Simpson. Mycosphaerella leaf disease does not appear
to cause much damage but its presence could constitute a potential threat.
IMPROVED IDENTIFICATION AND DETECTION
Difficulties in taxonomic identifications have led to inaccurate reports of the incidence
and impact of different species. The interpretation and, most importantly, comparison of
much past research are problematic. Accurate, rapid, and cost-effective molecular tools
provide a valuable link in the differentiation of fungal associations and highlight the
potential for detecting multiple pathogenic species simultaneously occupying the same
niche. Nested PCR technology has recently been adapted to detect five of the most
Mohammed et al. — Mycosphaerella leaf diseases
365
pathogenic and commonly identified species in Tasmanian E. globulus and E. nitens
plantations (Glen, Langrell, Tommerup, Smith & Mohammed unpubl. data). Mycosphaerella
spp. can be detected and discriminated in 25- to 200-mm2 samples of leaf, and in stem
slivers with or without visible lesions. Up to five Mycosphaerella spp. occurred together,
even in small leaf samples, and up to three were found in small samples without
macroscopically visible lesions. The detection of Mycosphaerella species from lesions
which are too immature to produce ascospores also opens up the possibility of using the
nested PCR technology to identify species at pre-visual and pre-necrotic stages, and to
develop a predictive tool for plantation management months in advance of the current
ability to identify Mycosphaerella leaf disease in plantations. The detection technology
applied to epidemiological research would greatly enhance the development of accurate
early-warning disease-forecasting systems. Whilst there is limited knowledge of the
pathogenicity of some Mycosphaerella species, the effects of a complex of species within
a leaf and within a lesion are unknown and require investigation.
RISK AND IMPACT MODELLING
Near-complete defoliation certainly captures the attention of forest managers but it is
the impact of a range of damage levels on growth rates and wood quality that is the key issue
in intervention decisions.
There was an attempt to establish E. globulus plantations in north-western Tasmania in
the late 1970s but planting was discontinued after 2 years because of unacceptably high
damage from Mycosphaerella leaf disease (David de Little pers. comm.). The high springsummer rainfall event that led to severe Mycosphaerella leaf disease in this initial period
of plantation development has recently been calculated by Wardlaw as a 1 in 25-year event.
This level of risk today would be considered acceptable for short-rotation high-value crops.
The preference for planting E. globulus on non-frost-prone sites because of its higher
pulp yields led Forestry Tasmania to plant E. globulus in 1997 in the Circular Head area of
Tasmania instead of E. nitens which is less susceptible to Mycosphaerella leaf disease.
Assessments of crown damage in 2002 by Wardlaw found severe Mycosphaerella leaf
disease (>50% leaf area loss) in nearly 50% of 2-year-old plantations in the Circular Head
area. The spring-summer rainfall event of 2002 corresponding with epidemic Mycosphaerella
leaf disease was calculated to be a 1:3.3 year event. Forestry Tasmania has ceased planting
E. globulus in north-western Tasmania until MLD can be managed.
A very small number of empirical studies have been done to measure the impact of
Mycosphaerella leaf disease on eucalypt growth. Defoliation levels of 25% were shown to
reduce wood volume in E. nitens infected with Mycosphaerella spp. in South Africa
(Lundquist & Purnell 1987). Carnegie et al. (1998) maintained that levels of diseased leaf
area as low as 10% result in up to a 17% reduction in the height of E. globulus plantation
trees. Since the first study was not sufficiently similar to the disease syndrome on
E. globulus, and the second did not measure growth for a sufficiently long period to allow
confident predictions of impact, we have recently established two long-term impact trials
in Tasmania:
•
An exclusion trial is measuring the impact of one or two light epidemic events on the
growth of E. globulus (between ages 1 and 2);
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New Zealand Journal of Forestry Science 33(3)
•
Growth plots have been established in two adjacent compartments that suffered
contrasting damage. One plot escaped epidemic disease, and the other suffered severe
disease (>70% crown loss) during its second growth season.
In the absence of immediate empirical data we have to resort to best-guess predictions
using growth models and extrapolated impacts based on empirical data for other pests.
More recently we have used process-based growth modelling (Sands et al. 2000; Pinkard
& Battaglia 2001; Battaglia et al. 2002).
The economic performance of different disease and management scenarios was
modelled by Wardlaw using stand management software linked to an E. globulus growth
model based on sites in northern Tasmania (peak mean annual increment (MAI) varying
from 22.5 to 32.5) pruned for solid wood, thinned at age 9 years, and harvested at age 22.
Two 50% bottom-up defoliation events (at ages 2 and 3) were predicted to reduce net
present value (NPV) from $1099 to $60/ha on high-quality sites targeted for sawlog
regimes.
While a reduction in tree growth is the usual consequence of loss of leaf area, the initial
responses affect basic physiological processes in the host. Photosynthetic responses are
likely to vary between defoliation due to insects, to pruning, or to leaf fungal infection.
Defoliation events in E. globulus (pruning / simulated insect defoliation) result in increased
photosynthetic response in residual foliage (Elek 1997; Pinkard et al. 1998). However, in
preliminary investigations, no compensatory response has been measured in leaves that
have lost functional leaf area due to necrotic lesions caused by Mycosphaerella spp.
(Pinkard unpubl. data). These differences in response are likely to affect source/sink
relationships and influence the partitioning of biomass. The most recent dynamic growth
model, CABALA, is particularly well suited to investigating the effects of diseases on
growth (Battaglia pers. comm.). Biomass allocation is linked strongly to the extent to which
resources limit growth, and the biomass of roots and foliage determines the rate at which
these resources can be acquired. The model predicts a number of stand components other
than wood volume, such as leaf area index, crown length, and the distribution of tree sizes.
These can be used to measure the impact of disease incidence. Furthermore the linkages
between capture of resources and the processes of allocation mean that the model has the
capacity to deal with or be adapted to the impact of disease on tree function. We have used
CABALA to model the effect of a 50% bottom-up defoliation of a 50-ha plantation on a
high-quality site in western Australia (MAI 31.5 m3/ha) grown for pulpwood on a 10-year
rotation. A single defoliation event decreased the value at harvest by $424/ha. We are also
applying CABALA to calculating leaf wetness (“water-holding capacity” of the canopy)
to better predict risk on any one site.
DISEASE ASSESSMENT
In a multi-disciplinary research programme such as the one we are conducting it is
essential that there is a common understanding and language to describe and measure crown
damage — that caused by Mycosphaerella spp. and by other biotic damaging agents.
The description of damage must be accurate and must include quantitative and
qualitative assessment of the type of damage (defoliation, necrotic lesions), location in the
crown (e.g., top-down, bottom-up), and temporal processes (blighting versus senescence
responses). Visual standards have been developed to provide precise and repeatable
Mohammed et al. — Mycosphaerella leaf diseases
367
measures of such damage. Assessment has to be carried out at both tree and stand levels.
A group of forest pathologists and entomologists in Australia are, as a matter of priority,
promoting national standards for the assessment of a crown damage index (CDI) on young
eucalypts (Stone et al. 2000, 2001; Stone, Matsuki, & Carnegie, 2003; Stone, Wardlaw,
Floyd, Carnegie, Wylie & Little 2003). The CDI is a single value, which represents the total
amount of damage present on a tree. The three general categories to calculate this value are
considered to be:
(1) necrosis,
(2) discoloration, and
(3) defoliation.
However, in more specialised assessments these can be split into specific categories. For
example, if a company was concerned about spread of Mycosphaerella leaf disease, and the
field staff could easily differentiate the symptoms, we could separate the necrosis
measurement into two scores (Mycosphaerella leaf disease necrosis, and other necrosis)
without compromising the final CDI score. For each category an incidence (percentage of
leaves affected in the tree crown) and a severity (percentage of leaf area damaged on
affected leaves) are estimated. A detailed Mycosphaerella leaf disease visual standard
(developed by Smith et al. in prep.) is used to obtain more accurate results (Stone, Matsuki,
& Carnegie 2003).
We have tested the accuracy, repeatability, and subjectivity of assessing Mycosphaerella
leaf disease and other damage at tree level to ensure the reliability, objectivity, and
repeatability of the crown damage index method (Smith et al. in prep.). Nine assessors, with
varying levels of experience, estimated damage on three plots of 50 trees each to obtain an
understanding of the subjectivity of assessing damage caused by insects and fungal
pathogens (e.g., Mycosphaerella spp.). The repeatability of estimates by the same assessor
was determined by estimating damage in the same plot of 50 trees in the morning and in the
afternoon. Information on the accuracy of estimates was achieved by destructively
sampling nine of the assessed E. globulus and measuring damage levels. The most
experienced assessors provided the most repeatable estimates and were generally the most
accurate. The incidence of foliar necrosis was the least subjective measure, while defoliation
was the most subjective and the least accurate of the indices measured. All assessors,
regardless of experience, were able to predict the crown damage index to within 12%.
Software that provides diagnostic assistance, training, quality assurance, and standardisation
for forest health research projects and surveys in sugar maple (Acer saccharum Marsh.), red
maple (Acer rubrum L.), black cherry (Prunus serotinia Ehrh.), white oak (Quercus alba
L.), and northern red oak (Quercus rubra L.) has been developed in Canada (Nash et al.
1992). We recommend that similar assessment-training software be developed for application
to the health assessment of eucalypts.
While field inspections enable the accurate identification of the damaging agents, the
ability to objectively quantify the spatial extent of damage and the impact on stand
productivity is more limited. In order to develop our decision-support models that provide
management with options to respond to changes in plantation health, there is a need for
quantitative data on tree health and condition. The application of high-resolution,
multi-spectral, reflectance imagery offers a means to obtain spatially-explicit data on the
physiological status of plantations (Martin & Aber 1996).
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New Zealand Journal of Forestry Science 33(3)
The integration of digitised canopy condition coverage with other physical and
environmental GIS layers presents the real possibility of spatial modelling of site-specific
classification and health risk ratings (Stone, Wardlaw, Floyd, Carnegie, Wylie & Little
2003). We are currently investigating the ability and operational feasibility of remote
sensing to determine Mycosphaerella leaf disease severity levels and the physiological
status of diseased trees.
CONTROL OPTIONS
Having predicted a high risk of recurrent epidemic disease and substantial economic
losses, the next challenge is to identify possible approaches to manage the disease. The
range of options in forestry is no different from agriculture but there are significant
constraints in their practical implementation.
Exclusion / Eradication
Exclusion / eradication is impractical — significant Mycosphaerella pathogens are
already widely dispersed. New introductions in Australia would be exceedingly difficult to
detect and map.
Chemical
Fungicides are useful to control Mycosphaerella leaf disease in the nursery (Dick &
Gadgil 1983; Carnegie 2000) but are not an environmentally or economically viable option
in large-scale plantations. For experimental purposes, exclusion in the field can be
achieved, weather and location permitting, with 2- to 3-weekly spraying of a common
fungicide such as benomyl. Preliminary trials by the Forest Research Institute, New
Zealand, found that two relatively new fungicides (Flusilazole and Azoxystrobin) showed
promise for the control of M. cryptica on 2- to 3-year-old E. nitens (Dick pers. comm.).
Included in the trials at the Forest Research Institute was the environmentally benign,
chemical, plant-defence activator phosphonate which has been sprayed aerially in National
Parks and World Heritage areas to control Phytophthora spp. If effective, but nonphytotoxic, levels can be applied then this chemical, or similar plant defence activators such
as Benzothiadiazol (Bion®), could offer protection for a considerable period of time as they
operate by inducing host resistance.
Resistance
There are some clear prospects with inter-specific differences already widely used on
high-risk sites (e.g., the use of E. nitens in north-western Tasmania). Intra-specific
differences exist but have yet to be exploited operationally.
We examined the quantitative genetic variation in susceptibility to infection by M.
nubilosa in a genetically diverse population of E. globulus families growing in a field trial
in north-western Tasmania. The trees were 2 years old and still in the juvenile foliage stage
when a heavy epidemic of M. nubilosa occurred. Disease incidence and severity were
assessed on juvenile foliage. Disease incidence was uniform across the trial, and the mean
leaf area damage was very high at 34%. Significant genetic variation in susceptibility was
Mohammed et al. — Mycosphaerella leaf diseases
369
detected, with a narrow-sense heritability of disease severity (0.6) being the highest yet
reported for Mycosphaerella leaf disease of eucalypts. We followed the effects of this
disease outbreak on growth up to age 7 years and found that M. nubilosa damage had a
significantly deleterious impact on tree growth at both the phenotypic and genetic levels.
At age 7, the top 10% of families had a mean diameter at breast height 20.8% greater than
the trial mean. Approximately half of this gain would have been achieved by early selection
for disease resistance (9.1%) or height (11.0%) at age 2, with a time advantage of 5 years.
This is similar to the selection of above-average families. It is likely such gains would be
reduced in homogeneous plantings of resistant genotypes, or if genotype × environment
interactions are significant. Nevertheless, a large component of this gain is likely to be due
to disease resistance per se, and collection of seed from resistant seed orchard parents offers
the potential for rapid gains in productivity in plantations at risk of disease.
Silviculture
Silvicultural treatments are considered to offer good prospects for control of
Mycosphaerella leaf disease — they are operationally feasible and potentially economically
viable. However, their effectiveness needs to be demonstrated experimentally.
There is some evidence that better nutrition may help to prevent or offset the effects of
biotic damage (e.g., Stone & Birk 2001; Stone 1993; Carnegie & Ades 2002) but this is far
from proven and the mechanisms behind such a response are not known. There is still much
debate associated with the outcomes of nutritional stress and insect herbivory. Silvicultural
treatments intended to improve tree vigour may also directly influence herbivorous
populations, either positively or negatively. Sap-sucking insects, aphids in particular, show
a positive response to nitrogen fertiliser. However, fertiliser application is perhaps the
silvicultural option with most promise in countering damage associated with foliar
pathogens or insect defoliation. It is well known that fertiliser treatment, in the absence of
other site limitations, promotes crown development, an option largely untested for reducing
the impact of fungal infections and chewing insects. Any additional resistance or accelerated
onset of more-resistant adult foliage is a bonus where Mycosphaerella leaf disease is
concerned.
On sites with sub-optimal soil nutrient reserves we find different responses to
Mycosphaerella leaf disease that suggest early secondary fertiliser application may be a
useful management tool. Height and diameter growth of trees planted in windrows is
insensitive to the severity of disease, whereas trees planted in the bays between windrows
record significant reductions in height increment as disease severity increases. Trees
planted in windrows do not appear to display premature senescence of spotted leaves.
There is little known about the physiological effects of plant nutrition on host response
to leaf infection and defoliation. A better understanding of the role of nutrition in such
responses may provide operationally feasible cultural controls for use in young plantations.
CONCLUSIONS
The traditional approach using empirical studies can predict (realistically) only within
the same range of conditions. Our studies on Mycosphaerella leaf disease on Eucalyptus
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globulus are being linked with a process-based model called CABALA being developed by
the Co-operative Research Centre for Sustainable Production Forestry in Hobart. This
allows the effect of damage on tree physiology to be linked with growth responses. Using
Mycosphaerella leaf disease as a case study will, we hope, allow realistic scenario-building
with the potential to more reliably predict the impact of similar damage caused by other
pests and pathogens and the effect of modifying silvicultural prescriptions, without the need
to resort to individual empirical studies.
ACKNOWLEDGMENTS
The authors would like to thank the following for assistance in the development of ideas and
concepts in the preparation of this paper: Dr Chris Beadle (CSIRO-FFP, Hobart) and Dr Christine
Stone (Research and Development Division, State Forests of NSW, New South Wales).
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