Anatomy of the infected stem
It was observed that the percentage of parenchyma cells in infected wood
was higher than that on healthy wood (Figs 9). However, the percentage
of fiber cell, fiber diameter and length were significantly more on
healthy wood compared to that on infected wood (Fig. 10)
Discussion
The occurrence and spread of A. decurrens as an invasive species
in all ecosystems in MNVP after the eruption of Mount Merapi have been
supported by several researchers (Lymberty et al., 2014 and Okoli et
al., 2017). However, the ecological impact of the species on the unique
successional processes in the post-eruption ecosystems around Mount
Merapi is only poorly known.
Ceratocystis fimbriata is proved to be the pathogen associated
with gummosis in A. decurrens. Ambrosia beetles
(Euwallacea sp.) which bore holes in the stem facilitate
infection by C. fimbriata. As already discussed, C.
fimbriata is a pathogen of several crop plants and it is widely
distributed in the tropics and subtropics (CABI, 2014). It has been
recorded on A. decurrens in Brazil
(Ribeiro
et al. (1988). The occurrence of the pathogen on A. decurrens in
MNVP poses threat to several crop plants in Indonesia.
In MNVP, although most trees displayed severe gummosis with 3 to 30
wounds per individual stem, the trees appeared healthy, with straight
stems, green canopy, and good performance in terms of height and
diameter compared to uninfected trees. The normal diameter of 5- yr-old
of healthy A. decurrens ranged from 9.2 – (Okoli et al. 2017),
while in MVNP the mean diameter of gummosis affected trees was already
at 4 years. This indicates that the gummosis had no impact on the
diameter growth of A. decurrens at MVNP.
The increased number of parenchyma cells in the infected wood and the
healthy growth of trees despite gummosis indicate that the parenchyma
cells aid in storage, conversion, and active transport of nutrients in
the gummosis affected trees (Schwarze et al., 2004). In addition,
parenchyma cells can also maintain meristematic activity such as wound
healing and regeneration of the young cells. However, A.
decurrens trees infected by C.fimbriata in the Capão Bonito
region, Brazil exhibited wilting, branch drying, wood splitting and gum
exudation which resulted in tree mortality (Ribeiro et al., 1988). The
difference here is that while A. decurrens trees in Brazil were
cultivated in plantations, trees in MVNP were naturally regenerated
under nutrient poor soil and adverse climatic conditions. Thus, the
trees in MNVP may have attained resistance towards insect pests and
pathogens. The monoculture of A. decurrens in plantations also
promotes disease severity and spread. However, strength properties of
infected trees in MNVP are significantly poor compared to healthy trees
since infection affects fiber quality.
Mitchell et al. (2010) have reported that species with high populations,
such as invasive species, are expected to exhibit greater accumulation
of pathogens over time in comparison to species with thin populations.
And, over time, pathogen accumulation may have little or no effect on
invasive species due to tolerance, compensation, or phenotypic
plasticity (Gilbert and Parker 2006; Alexander 2010). In certain other
cases, many invasive species exhibit substantial phenotypic plasticity
such that a reduction in population density has little effect on biomass
or seed production per unit area. Given the theoretical and empirical
demonstrations of the negative effects of pathogen build-up (Clay and
Kover 1996; Mordecai 2011), this outcome may seem unlikely, although it
is possible.
The vertical position of gummosis symptoms, which were abundant on the
lower stem and comparatively less on the upper stem and stem surrounded
by the crown, indicate that formation of the wound and subsequent
infection by Ceratocystis typically initiated from the lower part
of the trees. This observation suggests that ambrosia beetles (e.g.,Euwallacea sp.) which bore in to the xylem of trees can serve as
a vector for Ceratocystis spp. (Somasekhara, 1999). The frass
which cling close to the holes or accumulate on the bark and/ or at the
base of the tree may help spread of the pathogen (Paine et al. 1997; Six
2003; Harrington 2005).
According to Halloin (2003) and Lieutier (2004), bark beetles generally
oviposit at a location about 90 cm above ground (on pine trees) which
show that boring by the beetle tends to occur near the bottom of the
trees or the lower part of stem. Also, bark beetles locate mates and
attract or repel other individuals of the same species by emitting
species-specific pheromones (Sanborn (1996). Halloin (2003) observed
that when the beetles find a suitable host tree, they will release
aggregating pheromones to attract other beetles enabling a “mass
attack” that can overwhelm defenses of an otherwise healthy tree. These
observations will explain the more clustered spatial distribution of the
trees affected by gummosis in this study. Also, the study has shown that
the number of trees with gummosis symptoms decreases with increasing
distance between infected trees. The infection becomes successful when
the beetles releases the pheromones and along with it introducesCeratocystis which blocks the sapwood and weakens the tree. The
stress caused to trees caused by the pyroclastic flow can be another
reason for the susceptibility of the trees to Ceratocystis.
Although C. fimbriata does not impact growth of the invasiveA. decurrens at MVNP, the fungal inoculum poses a threat to other
plants within successional processes of the recovering ecosystem.
Invasive species are known to possess certain chemical weapons that
provide a selective advantage over their competitors (Callaway and
Ridenour 2004). It thus appears that the tolerance of A.
decurrens to C. fimbriata allow it to compete more successfully
as invasive species within MVNP ecosystem.
To conclude, the challenges here are complex, on the one hand the growth
and spread of A. decurrens is to be managed and on the other,
growth of native species needs to be promoted in the MVNP area by
protecting them from the invasive plant and the pathogen which occur on
it. Considering the highly successful establishment and spread ofA. decurrens , attempts to manage it and reclaim the land in the
MVNP area for regeneration of native species will be an onerous task
unless supported by the Government, land managers and the public, alike.
Conclusion
Ceratocystis fimbriata was proved to be the causal organism of
gummosis on A. decurrens trees that invaded MVNP ecosystems
following eruption of the Mount Merapi volcano. Four year after
eruption, the incidence of gummosis on the trees increased from 80 to
100% within a period of 6 months, with most symptoms located on the
lower part of the stem, followed by the upper part and on stem around
the crown. This positioning of infection indicated that the vector ofC. fimbriata , viz., Euwallacea sp. (ambrosia beetle),
initiated boring the tree at its base resulting in initiation of
infection there. Although all the A. decurrens tree stems
exhibited gummosis with number of gummosis wounds ranging from 3 to 30
per tree, most trees remained healthy and continued to grow. The tree
survival and growth is apparently due an increase in the number of
parenchyma cells in the wood which aided transport of nutrients within
the tree. The mean distance between infected trees in the study plots,
over a 6-month period, was , but decreased 1- with the disease progress
and spread. Management of invasion and spread by A. decurrensposes a challenge to all concerned due to the unparalleled invasion
success of the species and the threat from by its gummosis pathogen to
native species.
Authors’ contributions
SR set up the research methodology and led the writing of the
manuscript; RGP and JM collected the data and analyzed the data, MAI and
WDN contribute to the writing of the manuscript. All authors contributed
critically to the draft and gave final approval for the publication.
Acknowledgements
We thank the Higher Education Indonesia and the Educational Development
Fund Universitas Gadjah Mada year 2016 for financial support. Dr.
Istiana Prihatini is thanked for kindly sharing part of the laboratory
work with the lead author. Thanks are also for Dr. Ned B. Klopfenstein,
and Phill Cannon, Research Plant Pathologists, Forest Service, Rocky
Mountain Research Station, USA for advice and helpful suggestions.
Data Accessibility:
- DNA sequences: GenBank accession MH863157
- Other data uploaded as online
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