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:
References
Adams, A.B., Dale, V.H., Kruckeberg, A.R., & Smith, E. (1987). Plant survival, growth form, and regeneration following the May 18, 1980, eruption of Mount St. Helens, Washington. Northwest Science6,160–170.
Alexander, H.M. (2010). Disease in natural plant populations, communities, and ecosystems: insights into ecological and evolutionary processes. Plant Disease 94,492–503
Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D.J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25,3389-3402.
Barnes, I., Roux, J., Wingfield, B.D., Dudzinski, M.J., Old, K.M., & Wingfield, M.J. (2003). Ceratocystis pirilliformis , a new species from Eucalyptus nitens in Australia. Mycologia 95, 865-871.
Benson, D.A., Cavanaugh, M., Clark, K., Karsch-Mizrachi, I., Lipman, D.J., Ostell, J., & Sayers, E.W. (2017). GenBank. Nucleic Acids Research 45, 37-42.
Boucher, C. (1978). Black wattle. – Stirton, C.H. (eds.). Plant invaders, beautiful but dangerous . Department of Nature and Environmental Conservation of the Cape Provincial Administration, Cape Town, pp 48-51.
CABI Crop Protection Compendium. ”Ceratocystis fimbriata. CABI Publishing. (2004) . Retrieved 20 October 2014.