The Spread of Ganoderma From Infective Sources in The Field and Its Implications For Management of The Disease in Oil Palm

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8
J.
Spread
FloodofetGanoderma
al. from Infective Sources in the Field

The Spread of Ganoderma 8


from Infective Sources in the
Field and its Implications for
Management of the Disease in
Oil Palm
J. Flood1, Y. Hasan2, P.D. Turner3 and
E.B. O’Grady1
1CABI Bioscience, Egham, UK; 2Bah Lias Research Station,
P.T.P.P. London, Medan, North Sumatra, Indonesia; 3PO Box
105, Quilpie, Queensland, Australia

Introduction
Basal stem rot (BSR), caused by species of Ganoderma, has been recognized as a
serious disease of oil palm (Elaeis guineensis) for over 80 years and has caused
severe economic loss in Malaysia (Turner, 1981; Singh, 1991; Ariffin et al.,
1996) and North Sumatra, especially during the past 30 years (Hasan and
Turner, 1998). Initially, the disease was considered to affect only old palms (at
least 25 years old) but, with successive palm generations on the same land, a
higher disease incidence has been observed and the symptoms occur earlier
with each replanting. For example, in Sumatra, where replanting was con-
ducted by pushing over the old stand, with no attempt to remove BSR-infected
tissues, young replanted palms have died from the second year onwards after
planting. Economic loss may begin to occur within 10 years and severe loss
after 15 years; the normal life span of a planting of oil palm would be 25–30
years. Where this phenomenon has occurred, it has generally been accepted
that there has been an increase in available inoculum from the previous palm
planting (Turner, 1981). Thus, efforts to manage the disease have been
directed largely towards disease avoidance through reducing the amounts of
potential infection sources for the replanting at the time of clearing the old
stand (Singh, 1991). In Malaysia, the benefit of this clean-clearing approach
over no disease avoidance measures has been demonstrated (Hashim, 1991).
However, the total removal of all infective tissues from an old stand with a high
©CAB International 2000. Ganoderma Diseases of Perennial Crops
(eds J. Flood, P.D. Bridge and M. Holderness) 101

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102 J. Flood et al.

disease incidence is a practical impossibility, and so the aim has been to con-
centrate on removal of as many of the larger tissue sections as economically
feasible. To investigate the efficacy of sanitation in BSR management, a series
of trials was undertaken at Bah Lias Research Station (BLRS) of P.T.P.P.
London in North Sumatra, Indonesia over a period of several years. The trials
were designed to assess the relative importance of various tissue remnants
from the old palm stand as potential sources of inoculum at replanting (Hasan
and Turner, 1998) so as to make practical recommendations for management
of the disease in Sumatra.
The trials were set up as to be sufficiently large to overcome any variations
in BSR inoculum, with each treatment being replicated at different sites in the
plantation. Six-month-old seedlings were used to bait the Ganoderma-infected
material. External leaf symptoms developing on these bait seedlings were
recorded for the duration of each trial, while at the end of each trial, all
seedlings were examined internally for Ganoderma infection by destructive
sampling and plating to Ganoderma-selective medium (GSM) (Ariffin and Idris,
1991). Each experimental plot was isolated by a deep trench to increase the
likelihood that any infection recorded was derived from the tissue being tested
and not from an outside source, but more recently, molecular fingerprinting
techniques (Miller et al., this volume; Bridge et al., this volume; Rolph et al., this
volume) became available which allowed confirmation of the origin of the
pathogen in infected seedlings.

Stump Tissues
A stump comprises the base of the palm, or bole, and the thick crust of roots
immediately surrounding it. Stumps are usually recognized as major sources of
BSR. The first trial compared BSR stumps, prepared by felling diseased palms
about 20 cm above the ground (standard practice), as an inoculum source
with stumps derived from healthy palms. Around each stump eight bait seed-
lings were planted. An additional treatment, planting additional seedlings
immediately outside the plot isolation trench and isolating these by a further
trench 1 m from the inner trench, in order to emphasize disease origin, was
added. Each treatment was replicated eight times at different sites. Six months
after planting, a small number of seedlings began to exhibit disease symptoms
and by the end of the 28-month trial period, 76% of all bait seedlings showed
symptoms; Ganoderma was isolated from these seedlings. In comparison, seed-
lings planted outside the first trench and within the second isolation trench
perimeter showed very little infection – only 1.6% of these seedlings were
diseased and, at 80% of the replicate sites, these seedlings exhibited no
symptoms at all. No disease was recorded in bait seedlings planted around
healthy palm stumps within the period.
Another trial aimed to assess the effect of stump size on disease incidence.
Additional treatments in this trial were comparisons with stumps derived from

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Spread of Ganoderma from Infective Sources in the Field 103

healthy palms and the effects of pre-felling poisoning by paraquat, using 60 ml


per palm Gramoxone which was injected into the trunk. Stump size was found
to exert a marked influence on disease occurrence, with more bait seedlings
around smaller, lower stumps (20 cm high) exhibiting disease symptoms after
2 years than those around larger, higher stumps (50 cm high). Rate of
decomposition and bait seedling root ingress into Ganoderma-colonized tissues
would appear to be the most likely explanations for the difference. The effects of
poisoning, which had accelerated tissue breakdown, supported this, with more
seedling infection recorded around larger stumps where poisoning treatment
had been carried out.
The importance of inoculum sources at different soil depths adjacent to
BSR-infected stumps, which is of considerable relevance to sanitation
practices, was also investigated. Thus, soil and palm tissue adjacent to BSR-
infected stumps were removed to one of the following depths: 20, 40, 60, 80
and 100 cm. Eight replicate bait seedlings were planted at each depth and
these treatments were compared with diseased stumps that were undisturbed
after felling (no soil or tissues removed) and sites around healthy palms
excavated to a depth of 60 cm. In the absence of any sanitation, 75% of
seedlings had become infected and 97% of replicate sites had infected plants
within 2 years of planting (Table 8.1). In comparison, disease incidence in the
baited seedlings decreased to 21% where soil and debris had been removed to a
depth of 60 cm, and no disease was recorded where soil and debris had been
removed to 80 or 100 cm (Table 8.1).
In an extension of this trial, the same sites were replanted with bait
seedlings after 2 years and no disease was recorded at any depth 2 years later.
Similarly, when new bait seedlings were planted around previously highly
infective diseased stumps after 2 years, none of these bait seedlings developed
symptoms. Even after 2 further years of recording, these seedlings remained
symptomless, which would suggest that the potential of these stumps to act as
sources of inoculum had declined after 2 years. Data of percentage infection
over time at two sites (Table 8.2) further supported the view that fewer seed-
ling infections occurred after 20–24 months. Some variation between sites is

Table 8.1. Effects of the removal of soil and palm tissues from around healthy
basal stem rot (BSR)-infected stumps on disease incidence after 24 months.

Depth of bole % Replicate sites with % Seedlings


Disease status removed (cm) infected seedlings infected

BSR 0 97 75
BSR 20 85 58
BSR 40 70 28
BSR 60 55 21
BSR 80 0 0
BSR 100 0 0
Healthy 60 0 0

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104 J. Flood et al.

to be expected since the amount of infective tissue within stumps and its
location in relation to seedling root contact will differ considerably, as will the
rates of subsequent decay.
During the course of these trials, molecular fingerprinting techniques
became available for Ganoderma and were used to confirm the origin of the
Ganoderma from infected bait seedlings. Material was collected from diseased
seedlings, stump tissues and sporophores growing on the stumps and
isolations made on GSM. DNA was extracted from pure cultures (Miller et al.,
1999) and purified DNA samples tested with the ITS3/GanET primer (Bridge
et al., this volume) to check their identity. All isolates were positive with the
ITS3/GanET primer, confirming that the pathogen had been isolated from
the various tissues (Fig. 8.1). Mitochondrial profiles were generated using the
enzyme HaeIII as the restriction enzyme (Miller et al., 1999; Rolph et al., this
volume) and revealed that identical profiles were present in the BSR stumps
and the infected bait seedling material (Figure 8.2).

Table 8.2. Percentage of total bait seedling infection


appearing around basal stem rot stumps over time.

% Seedling infection
Months after
planting Site A Site B

6–8 8 11
9–12 45 32
13–18 20 35
19–24 20 14
25–28 7 8

Fig. 8.1. Confirmation of the presence of the pathogen from stump tissues and
infected seedlings.

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Spread of Ganoderma from Infective Sources in the Field 105

Fig. 8.2. Mitochondrial DNA restriction fragment length


polymorphisms of Ganoderma isolates from an infected
basal stem rot stump and from a baited infected seedling
planted near the infected stump.

As mitochondrial (mtDNA) inheritance is believed to be unilinear (Forster


and Coffey, 1990), isolates from the same sibling family would therefore have
the same profile. However, generally, mtDNA profiles are highly variable in
Ganoderma isolates, even from the same and adjacent oil palms (Miller et al.,
1999). Thus, identical mtDNA profiles from BSR-infected stumps and from
infected bait seedlings may indicate that mycelial spread or root-to-root con-
tact has occurred, but, equally, the role of basidiospores cannot be ruled out
(Miller et al., 1999). To clarify this point, a third molecular profiling technique
was used, namely amplification fragment length polymorphisms (AFLPs), as
described by Vos et al. (1995). This technique assesses the total cellular DNA
profile (nuclear and mitochondrial DNA) and is a more stable and reliable
method of studying variation (Rolph et al., this volume). Identical AFLP profiles
were produced using several primers, including primer E (Rolph et al., this
volume) (Fig. 8.3) confirming that the baited seedlings were infected with the
same genotype as that in the BSR-infected stump.

Trunk Tissues
Unless trunks of the old palm stand are destroyed at the time of replanting, they
are usually windrowed, i.e. placed in rows. Such trunks are colonized by many
species of fungi, including Ganoderma. Trunks will also remain following a
number of estate practices, e.g. following underplanting, those excavated as
low-yielding, palms removed for thinning or road construction and excavated
diseased palms, and palms affected by upper stem rot (USR) often remain
standing for long periods, as do palms killed by lightning. The trials summa-
rized below assessed the significance of trunk sections as sources of BSR

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106 J. Flood et al.

Fig. 8.3. Amplification fragment length polymorphisms


from basal stem rot stump, baited seedling and
Ganoderma sporophore (fruit body) growing on the
infected stump.

following various treatments and compared these sources with BSR-infected


stumps. Palms were felled as close as possible to the ground and the trunk then
cut at 1 m and 4.75 m from the base, with the remainder being discarded. The
stump and each trunk section were isolated by trenches and bait seedlings
were planted close to the sections. Apparently healthy palms were also
included.
Stump tissues remained the most important source of BSR, with 27–38%
seedling infection occurring, and although the incidence of disease arising
from trunk sections was much lower (Table 8.3), this would remain of
considerable practical significance.
There was a marked increase over the 2-year period in the number of
infection foci on what had previously been considered as healthy stumps, with
the highest disease incidence (12%) being recorded where palms had been
poisoned before felling and where legume overgrowth had been successful.
The presence of diseased seedlings around what had previously been consid-
ered to be healthy palms would indicate that the pathogen is present in the
palm for what maybe a considerable time before symptoms are seen.
Infection rates of bait seedlings when planted around standing diseased
and apparently healthy palms were compared with that from stumps; the
infection rate of bait seedlings around standing palms was much lower
(Table 8.4). However, the period of infectivity of standing palms is likely to be
much longer, demonstrating the need to remove such palms in management
of the disease. Also, while diseased tissues appear to lose much of their infective
ability from about 18–20 months after felling, the majority of apparently
healthy stumps and trunks had yet to show the extent to which they would

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Spread of Ganoderma from Infective Sources in the Field 107

Table 8.3. Basal stem rot incidence in bait seedlings around oil-palm residues.

% Seedling % Seedling infection % Seedling infection


infection around around proximal around distal trunks
stumps trunks (stem) (stem)
Disease
status Treatment Yr1 Yr2 Yr1 Yr2 Yr1 Yr2

Diseased Nil 9 38 2 3 2 2
Diseased P 13 34 3 5 2 3
Diseased C 19 34 4 6 1 2
Diseased PC 17 27 4 5 5 6
Healthy Nil 0 6 1 1 1 1
Healthy P 1 9 2 3 1 1
Healthy C 0 7 5 6 4 4
Healthy PC 4 12 1 1 1 3

P, Poisoned before felling; C, legume cover.

become sources of disease at the end of 2 years (Table 8.4). However, from
the 2-year data alone, it is clear that under field conditions they will certainly
present a significant disease risk.
In another trunk treatment, pieces were cut to simulate shredding as a
clearing method, with and without poisoning prior to preparation. These were
either placed on the soil surface or buried at 20 cm deep. Both infected and
healthy trunk tissues were examined, with seedling baits used to detect BSR
in plots isolated by trenches. Both diseased and healthy shredded tissues can
give rise to disease after burial. Except in a single instance, superficially placed
tissues were not a disease hazard. In plots with buried tissues where disease
was recorded, sporophores of Ganoderma were produced on the soil surface.

Roots
The current recommendation for BSR sanitation procedure concentrates on a
1.5 m square centred on the point where the palm is planted. The assumption
has been that the remaining inter-space presents no serious disease hazard. In
a trial to examine this, areas between neighbouring diseased palms were each
divided into three equal parts and isolated by deep trenches. Bait seedlings
were then planted in each sector, as well as around the bases of the BSR-
affected palms. Similar sectors between apparently healthy palms were also
baited. In the BSR plots, Ganoderma fructifications developed on cut root
ends, signifying the presence of infected roots. The overall incidence of seedling
infection was low (4%) and was confined to the sectors closest to the diseased
palms, whereas 69% of bait seedlings planted around the main disease sources
became infected. No disease was recorded between healthy palms.

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108 J. Flood et al.

Table 8.4. Comparison of basal stem rot (BSR) in bait seedlings around standing
BSR and healthy palms compared with stumps, 2 years after treatment.

Standing palms Low stumps

Disease % Infective % Seedling % Infective % Seedling


status Treatment sites infection sites infection

BSR Nil 30 6 90 38
BSR P 40 10 95 34
Healthy Nil 20 3 20 6
Healthy P 30 7 40 9

P, Poisoned.

Also, records of the production of Ganoderma sporophores on cut ends of


roots on the inside of isolation trenches from the depth trial (Table 8.1)
revealed that where no soil or palm tissues had been removed, 67% of all
replicate sites had Ganoderma sporophores, while where soil had been removed
to a depth of 60 cm, this had decreased to only 10%. Thus, diseased roots can
comprise a small, but still significant, source of BSR in a replant, although this
probably requires dense root aggregations.

Discussion
It is apparent from these results that, when suitable disease sources are
present, oil-palm seedlings can be attacked by Ganoderma soon after planting.
Disease development and overt symptom appearance will depend on the size of
the palm when it becomes diseased, its continued growth vigour and the size
of the inoculum. Small seedlings close to large disease sources are killed
rapidly. Larger, rapidly growing plants are also affected, but frequently do
not die quickly. Numerous investigations have reported that many infected
palms continue to grow well, often for very long periods, before the internal
BSR lesion becomes so extensive that visible external symptoms develop. This
explains why so many cases of BSR occur long after planting and also after
obvious sources of primary infection have disappeared.
Once a few palms in a field are infected it has been considered that further
colonization of palms in the field is due to root-to-root contact by the palms or
mycelial spread. Both Singh (1991) and Hashim (1994) reported the disease as
occurring in patches or groups, which would support palm-to-palm infection,
but this view has been challenged recently by Miller et al. (1999). Studies of
somatic incompatibility and mtDNA profiling of isolates taken from many
adult palms within two oil-palm blocks (Miller et al., this volume) revealed con-
siderable variation between isolates, and led to the conclusion that isolates
occurred as numerous distinct genotypes, even within the same palm. Thus,

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Spread of Ganoderma from Infective Sources in the Field 109

mycelial spread to adjacent palms or root-to-root contact was very unlikely.


Ariffin et al. (1996) similarly reported a high degree of heterogeneity between
isolates taken from adjacent infected adult palms. This contrasts with
other wood-rotting fungi, such as Heterobasidion annosum (Stenlid, 1985) or
Phellinus noxius (Hattori et al., 1996), where one clone of the pathogen can
extend over several metres. However, the preliminary mtDNA and AFLP
profiling described here has demonstrated that the same genotype is present in
the diseased stump and in baited seedlings. Thus, the experimental assumption
that the infected BSR stump acts as a direct source of infection to the young
seedlings was validated. Infection probably occurred due to the growth of seed-
ling roots towards the decaying stump which is a rich source of nutrients.
However, molecular analysis has only been conducted on a small number of
stumps, and other sources of infection for young seedlings in the field cannot be
ruled out. To date, the role of basidiospores has never been fully explained in
this disease. Thompson (1931) suggested that they were responsible for USR,
usually in association with Phellinus spp., but Turner (1965) failed to infect oil
palm following direct spore inoculation of cut frond bases, and Yeong (1972)
reported no infection following direct inoculation of oil-palm seedlings.
However, it is possible that basidiospores could infect palms indirectly, i.e. are
able to colonize debris which subsequently becomes the source of infection
for living palms (Miller, 1995). This would account for the heterogeneity
determined using molecular markers (Miller et al., 1999). Thus, much more
molecular analysis remains to be conducted – so far only diseased stumps
have been studied, but trunks and even roots can act as significant sources of
infection.
The investigations reported here have confirmed that the times of greatest
practical significance for the control of Ganoderma in oil palm are: (i) soon
after planting, when suitable inocula remain in the ground from the previous
planting (oil-palm stumps or root debris); and (ii) later in the planting cycle,
when root contact is made with Ganoderma-colonized sections of palm trunks
resting on the ground in rows (windrows). Results of this study would seem to
suggest that this danger extends over a much longer period when windrowed
palms are not poisoned prior to felling and are not covered by legumes to
accelerate decomposition.
Fungi that cause root disease frequently require substantial inoculum
potential before they are able to initiate infection and subsequently become
established within the host plant. Thus, infection must require either a block of
Ganoderma-colonized tissue of adequate size or a conglomerate of tissues, e.g. a
mass of infected roots, which collectively become an infection source. In the
trials summarized here, the importance of large blocks of inoculum is evident.
Bait seedling infection was very rapid when planted close to BSR-infected
stumps. Gradual removal of this source with increasing depth showed a clear
relationship between availability of infective material and both the occurrence
and incidence of BSR. This was not confined to the stump tissues. At a depth of
60 cm there was no mass of stump tissue, only a few infected roots, but these

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110 J. Flood et al.

root masses can become significant sources of infection. Even where a field that
has been carefully cleaned of debris at replanting, as the new seedlings grow,
more and more root debris is produced. This will include a large amount of root
material from self-pruning (Hartley, 1988; Jourdan and Rey, 1996) and large
numbers of fine quaternary roots are present in the upper layers of the soil. The
hypothesis that this material could become the substrate for basidiospore
colonization requires further study.
The depth factor poses considerable problems from the practical viewpoint
of sanitation at the time of clearing for replanting. Breaking up deeply located
root masses requires deep tining, for which equipment is not always available.
If seedlings are planted at the same points of former BSR palms, there is a
distinct possibility that their roots will soon encounter infective sources of
Ganoderma, and thus as much of the diseased stump tissue as possible should be
removed. However, further baiting using seedlings showed that these potential
BSR sources were less of a disease hazard after 2 years. This means that their
importance could be expected to be very much reduced, or even negligible, if
new palms are planted as far as possible from the old planting points. Their
disease potential would have greatly diminished by the time the roots of the
new planting reach the hazard sources, provided the old stand had been
poisoned before felling. Alternatively, delayed planting could be a useful
method of disease avoidance.
Windrowed palm trunks represent another significant problem, and the
same considerations apply to the necessity for planting as far away as possible
from windrows. The lateral extent of root development during immaturity
reaches roughly the edge of the canopy, meaning that it should take 2–3 years
before reaching this particular disease source if planted at the furthest possible
distance. An important observation is that the period over which windrows
remain a disease hazard is greatly reduced when palms of the old stand are
poisoned by paraquat prior to felling, and this effect is further enhanced
when they are cut into sections and with a thick overgrowth of legume cover.
Where there has been no poisoning, the tissues remain a disease hazard for
years. In such situations older palms of the replant become infected, with overt
disease symptoms only appearing long after the original infection sources have
disappeared.
One solution is to shred palm tissues so that they do not become BSR
sources over long periods, which is already a common practice in Malaysia but
not in Sumatra. However, even this does not provide a total answer to the
problem. Occurrence of BSR in bait seedlings, arising from buried, shredded
diseased and healthy trunk segments, was limited, but illustrated that the
technique still contains a degree of disease risk. Disease arising from
superficially placed segments was very slight and unexpected. It was in some
ways remarkable that in such segments, buried or superficially placed, disease
occurred at all, since many attempts at artificial inoculation of seedlings in
polybags using such tissues have failed. The appearance of Ganoderma sporo-
phores on the soil surface above buried BSR sections indicated that a sufficient

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Spread of Ganoderma from Infective Sources in the Field 111

mass of Ganoderma-colonized tissue can overcome the inhibitory effects in soil


which normally prevent its development there.
Another possible BSR control method for the future lies in the fact that
trunk tissues, in particular, support the rapid development of many fungi other
than Ganoderma, and this points to a possible biological control approach to the
windrow disease hazard problem. Rapid degradation of the windrowed tissues,
especially by fungi antagonistic to Ganoderma, would have obvious advantages
for BSR and Oryctes control. However, this approach needs more investigation,
not least because woody tissues contain very little nitrogen, this influencing
the extent of colonization by certain rotting microorganisms, so that manipu-
lation of the nitrogen status of the debris will need to be conducted (Paterson
et al., this volume).

Acknowledgements
This chapter is published with the permission of P.T.P.P. London, Sumatra,
Indonesia. The considerable assistance of field staff in the execution of trials is
gratefully acknowledged. The authors would like to thank the Crop Protection
Programme (CPP) of the Department for International Development (DFID) for
funding some of the research reported here, which was administered through
NRI (RNRRS Project 6628).

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