Changes of mycorrhizal fungal community occurring during the natural restoration after the chi-chi earthquake in Taiwan

Abstract

Arbuscular mycorrhizal (AM) fungi influence the plant establishment after disturbances, however, there were no reports on the succession of soil AM fungal communities after earthquakes. This study was carried out to monitor the changes of AM fungal species composition during plant succession after earthquakes. After a major earthquake, the ‘Chi-Chi’ event of 1999, a total of 4238 AM fungal spores belonging to 13 species were recorded. Higher AM fungal spore density was found in the crest area of the affected mountainside and the AM fungal community was significantly different between the crest and valley area. Scutellospora nigra, Acaulospora scrobiculata and Acaulospora tuberculata were dominant in the early succession stage. Glomus ambisporum, Glomus deserticola and Acaulospora mellea were more abundant in the late successional stage. These results demonstrated the dynamics of AM fungal community during succession and vegetation recovery.

Introduction

Arbuscular mycorrhizal (AM) fungi, which mutually associate with 70–90% of land plants (Smith and Read 2010), have the potential to increase nutrient and water availability, promote host plant growth and enhance tolerance of the plant to stresses (Miransari 2010; Smith and Read 2010; Wang et al. 2012). They can also contribute to soil aggregation by extra-radical hyphae and glomalin production (Rillig et al. 2002). Because of these potential benefits, AM fungi can influence plant performance, productivity, diversity, and community directly and indirectly (Klironomos et al. 2000; Kikvidze et al. 2010; Lin et al. 2015). AM fungi play a critical role in plant succession and assembly (Kikvidze et al. 2010; García de León et al. 2016), and they are important for the revegetation of disturbed areas (Asmelash et al. 2016).

Microcosm experiments (Grime et al. 1987; Vogelsang et al. 2006) and a field experiment (Yang et al. 2014) have found that the presence of AM fungi influence the diversity and composition of plant communities and revealed the importance of AM fungi for plant establishment during succession (Kikvidze et al. 2010). However, only a few early studies have described successional changes of the fungi during the development of plant communities (Allen et al. 1987, 1992; Warner et al. 1987). Recent studies have used a chronosequence approach to study the mycorrhizal succession (García de León et al. 2016; Krüger et al. 2017), but the shifts in AM fungal communities during succession still remain poorly understood (Dickie et al. 2013) and there is a lack of realistic, in situ field studies characterizing the succession of AM fungal communities.

Most studies of AM fungi during succession have focused on the proportion of root infection, with a few studies describing community composition. Reports have described compositional shifts in volcanic systems (Oba et al. 2004; Wu et al. 2007), after alteration of land use (Turrini et al. 2016; Koziol and Bever 2016) or after wildfire disturbance (Bellgard et al. 1994). Natural disturbances, such as earthquakes, fire, hurricanes, and tsunamis are important factors driving the ecosystem development (Attiwill 1994) that also deserve attention. As destructive disturbances, earthquakes result in the alterations of landscapes, landslides and the losses of vegetation cover and forest (Lin et al. 2005). In this context, the main aptitude of AM fungi is the mobilization and transport of mineral nutrients (particularly phosphorus) from soil micro-compartments that are not accessible to roots or root hairs (Karandashov et al. 2004). This property is likely crucial for enabling pioneer plants to survive the barren and arid environments that exist subsequent to powerful disturbances. However, to the best of our knowledge, there has been no previous research into the succession of AM fungi after earthquake events.

The Chi-Chi Earthquake that occurred on September 21, 1999, caused serious landslides and massive loss of vegetation cover in central Taiwan (Lin et al. 2005). Landslides in the Jiujiufong area were especially serious, causing a total area of 1025 ha to be exposed within several forest compartments (Huang 2002; Chen 2005). After the earthquake, 80% of the vegetation in the Mt. Jiujiufong area was destroyed, with most barren lands appearing at the crest of the mountain. This area has been designated as a natural reserve to conserve the natural recovery of plants on the landslide scars. The geological feature from Taiwan’s Central Geological Service shows that the stratification here was formed by gravel, rock and minor sandstone. Unique geographic feature and active plant succession have been observed at several landslide locations. Mycorrhizal fungi could facilitate the establishment of vegetation cover, and recovery of plant community after destructive disturbances. It is important to understand the predominance of AM fungi to assess their potential for restoration of degraded lands (Asmelash et al. 2016; Neuenkamp et al. 2018).

Traditionally, AM fungal diversity is investigated by observing and identifying the spores from soil. Recently, high-throughput sequencing platforms have become popular to study the biodiversity of AM fungi associated with plants (Turrini et al. 2016; Krüger et al. 2017). However, it is important to isolate AM fungal spores for further utilization, such as mycorrhizal inoculation or ecological restoration. In this study, the AM fungal community composition and diversity on the Mt. Jiujiufong landslide scars were described based on morphospecies. We monitored the composition of AM fungal communities in situ during plant community recovery and compared the AM fungal community of a crest area (bare land) to a valley (fertile land).

Materials and methods

Study area

Our study was conducted on the Mt. Jiujiufong, located at the border of Tsaotun and Guoxing townships in Nantou County, Taiwan. The study site was situated at 24°00’N, 120°45′E at 450 m above sea level. The climate data obtained from Taiwan’s Central Climate Bureau. The highest average temperature in this area is 34.5 °C in July; the lowest average temperature is 12.1 °C in February with relative humidity is ca. 86% overall. The average annual precipitation is 1800 mm. The geologic soil structure in this area derives from thick gravel and some sandstone; due to continuous weathering and erosion, the landform is cut into broken sections or fragments and the geographic structure is fragile.

After the Chi-Chi earthquake, most areas at the crest of the mountain became bare land and the vegetation was destroyed (Fig. 1a); access to the area has been restricted to permit natural recovery of plants for the landslide scars. During the initial recovery stage, pioneer species like Trema orientalis, Macaranga tanarius, Mallotus paniculatus,Sapium discolor, Rhus chinensis var. roxburghii were often found on the crest (Lin and Wu 2007). However, after fifteen years, Pinus taiwanensis has occupied and dominated the plant community (Fig. 1b); this was accompanied by plant canopy closure, plant litter and soil humus increased. In contrast, the area in the valley retained normal vegetation coverage after the earthquake. Shade-tolerant plants continued to occupy and dominate plant community in the valley (Lin and Wu 2007).

Fig. 1
figure1

After the Chi-Chi earthquake that occurred on September 21, 1999, most areas at the crest of the mountain became bare land and the vegetation was destroyed (a); after fifteen years, Pinus taiwanensis has occupied and dominated the plant community (b)

Experimental design, soil sampling and identification of mycorrhizal species

The AM fungal communities at Mt. Jiujiufong were investigated from August 2001 to September 2015. We investigated habitat effects on AM fungal community and compared the AM fungal species composition during the plant succession event after the Chi-Chi earthquake.

For habitat effects, four plots (10 × 10 m) were established in the crest area and three plots (10 × 10 m) were established in the valley. Soil samples were taken from these plots on 22 August 2001, 22 August 2002 and 7 November 2002. In the crest area, the vegetation was destroyed. The natural recovery of plants in the crest area was observed and recorded. To compare AM fungal species composition on the plant communities developing after earthquakes, in the early successional stage we monitored the AM fungal diversity and community each summer from 2001 to 2003 in the crest area. During this period, four to five plots were investigated. To avoid human disturbance, the study was temporarily suspended in 2003. The area was re-surveyed from 2014 to understand the recovery of the plant community and succession of the mycorrhizal community. In 2014 and 2015, the plot numbers were increased to 8 and 7, respectively.

In each plot, four soil samples were systematically taken from the topsoil (0–20 cm depth) and mixed into one pooled sample. A subsample of approximately 100 g soil from each pooled sample was then taken for identification and determination of spore numbers of each AM fungal species. AM fungal spores were isolated from the soil samples by wet sieving (Gerdemann and Nicolson 1963) and sucrose centrifugation (Jenkins 1964). To identify AM fungal species, the spores were mounted on the slides using polyvinyl alcohol with and without Melzer’s reagent (Morton 1988) according to the method of Schenck and Pérez’s Manual (Schenck and Pérez 1990) and the classification of the Glomeromycota (Schüßler and Walker 2010). Spores were examined microscopically and identified according to taxonomic criteria (Schenck and Pérez 1990; Oehl et al. 2011a, 2011b) and taxonomic information supplied by INVAM (2003).

Data analysis

Construction of a data matrix based on the diversity and abundance of AM fungal species was followed by square root transformations. The binary matrix was used to calculate the Bray-Curtis Similarity Index (Clarke and Warwick 2001) and to construct nonparametric multi-dimensional scaling (nMDS) plots using Primer 6 software (version 6. 1. 15; Primer-E Ltd., United Kingdom). Analysis of similarity (ANOSIM) was used to test hypotheses relating to community structure differences within and between sample groups, such as habitats and successional stages. This method allowed statistical tests of observed differences among groups of samples. All ANOSIM analyses used the Bray-Curtis index, permutations set at 999 at a p value of 0.05.

The major species driving distribution patterns of arbuscular mycorrhizal assemblages among habitats or successional stages were identified by similarity percentage analysis (SIMPER). The average dissimilarity among all pairs of samples between groups and the contribution to the relative dissimilarity were calculated and assessed by SIMPER. SIMPER analysis provided the percentage of contribution of each species that explain the dissimilarity observed among samples from different habitats or successional stage.

Results

Influence of habitats on AM fungal diversity and communities

A total of 4238 AM fungal spores were recorded from 38 soil samples, and 13 AM fungal species were identified (Table 1). The spore density of three dominant species (Acaulospora scrobiculata, A. morrowiae and Paraglomus occultum) at Mt. Jiujiufong were 127, 268 and 394 spores per 100 g bulk soil, respectively. There were eight AM fungal species (A. foveata, A. koski, A. scrobiculata,A. morrowiae, Diversispora spurca, Paraglomus occultum, Scutellospora pellucida and S. nigra) found in the crest area on 22 August 2001, four species on 22 August 2002, and four species on 7 November 2002. The AM fungal spore density in the crest on 22 August 2001, 22 August 2002 and 7 November 2002 was 593, 182 and 75 spores per 100 g bulk soil, respectively. During the same period of survey, 2 (A. morrowiae and S. pellucida), 3 (A. tuberculata,A. morrowiae and Scu. pellucida) and 2 (A. tuberculata and Scu. pellucida) species and 27, 63 and 24 spores per 100 g soil were found in the valley (Fig. 2). Comparing the two areas, higher AM fungal species and spore density were apparent in the crest areas (Fig. 2).

Table 1 Number of detected mycorrhizal fungal species and spores in the valley and in the crest area in Mt. Jiujiufong from August 2001 to September 2015, subsequent to the Chi-Chi earthquake event
Fig. 2
figure2

Spore abundance and AM fungal species richness in the crest and valley area of Mt. Jiujiufong after the Chi-Chi Earthquake event. Values are means; bars represent standard error of the mean

Acaulospora morrowiae was dominant in both areas. Paraglomus occultum and A. scrobiculata were the dominant species in the crest area, while S. pellucida was dominant in the valley area (Table 1). nMDS plotting (Fig. 3) and the ANOSIM test show that AM fungal community in the crest area was significantly distinct from the community in the valley area (p = 0.024). This result suggested that habitats influenced the AM fungal community. The SIMPER test showed that P. occultum, A. morrowiae,A. tuberculata, S. nigra and S. pellucida were the main contributors of variation between the AM fungal communities in two habitats, contributing 30.19%, 26.07%, 11.77%, 11.59% and 10.67% dissimilarity, respectively. Paraglomus occultum andS. nigra were found only in the soil from the crest area (Table 1). A. morrowiae and S. pellucida were found in two habitats; while the former had more spores in the soil from the crest area, the latter displayed the contrary trend (Table 1).

Fig. 3
figure3

Non-metric multidimensional scaling ordination of AM fungal communities from the crest and valley area of Mt. Jiujiufong after the Chi-Chi Earthquake event. Symbols represent two different habitats. Regular triangles represent AM fungal communities from the crest area. Inverted triangles represent AM fungal communities from the valley area

Successional dynamics of AM fungi after the earthquake

During the summers of 2001, 2002, 2003, 2014 and 2015, AM fungal species recorded in the soil from the crest area numbered 8, 4, 3, 6 and 6, respectively. AM fungal spore densities per 100 g soil in the same yearly samples were 593, 182, 7, 40 and 41 spores, respectively. AM fungal species richness and spore density tended to decrease from 2001 to 2003 and increase from 2003 to 2015. The nMDS plot revealed a clear contrast between the 2001–2003 and 2014–2015 successional stages in the structure of the AM fungal communities (Fig. 4). ANOSIM pairwise comparisons also indicated that AM fungal communities occurring in 2001, 2002 or 2003 significantly differed from the AM fungal communities during 2014 or 2015 (p < 0.05). However, the AM fungal communities observed during 2001, 2002, or 2003 did not differ from each other significantly and the AM fungal communities between 2014 and 2015 were not significantly different. Temporal community change occurred in two main phases in relation to the succession stage (Fig.4).

Fig. 4
figure4

Non-metric multidimensional scaling ordination of AM fungal community from different successional stages on the crest area of Mt. Jiujiufong after the Chi-Chi Earthquake event. Symbols represent AM fungal communities from different years: regular triangles, 2001; inverted triangles, 2002; squares, 2003; diamonds, 2014; circles, 2015

The SIMPER test showed that P. occultum and A. morrowiae were the main contributors of variation between the AM fungal communities in 2001–2003 and 2014–2015, contributing 28.32% and 19.77% dissimilarity, respectively. Paraglomus occultum andA. morrowiae were the most abundant spores in the crest soil sample and were found from 2001 to 2015. Both of their spore densities decreased over time (Table 1). Acaulospora scrobiculata and A. tuberculata were dominant in the early succession stage (from 2001 to 2003), and they were not recorded from 2014 to 2015 (Table 1). Glomus ambisporum, A. mella andG. deserticola were more abundant in the late successional stage, and not recorded during the early succession stage (Table 1). We also observed ectomycorrhizal fungi, including Suillus placidus, Pisolithus tinctorius and Amanita melleiceps, recorded for the first time in 2003, 2014 and 2015, respectively.

Successional dynamics of plants after the earthquake

A total of 19, 21 and 25 species of vascular plants was recorded in 2001, 2002 and 2003 respectively (Table 2). Eleven years later, a total of 9 species of vascular plants was recorded in 2014 and 2015 (Table 2). In 2014 and 2015, Pinus taiwanensis occupied and dominated in the crest area; this was accompanied by plant canopy closure, and an increase in plant litter and soil humus.

Table 2 Inventory of vascular plant species in the crest area in Mt. Jiujiufong from August 2001 to September 2015, subsequent to the Chi-Chi earthquake event

Discussion

In 1999, the Chi-Chi Earthquake resulted in landslides and caused a huge loss of vegetation cover in the crest area; there were no plants, litter or coarse woody debris covering the bare ground of the crest. However, the vegetation in the valley was not seriously affected. In 2001, there were more than 500 spores/100 g soil in the crest area and the majority of spores were the following AMF species, A. foveata, A. koski, A. scrobiculata,A. morrowiae, S. pellucida, S. nigra, D. spurca and P. occultum. Immediately after the disturbance, the bare ground in the crest area provided an empty niche for AM fungi and pioneer plants. Thereafter, pioneer plant species colonizing the crest area offered an increased rhizosphere area available for AM colonization and maintained higher AM sporulation than late successional plants in the valley, similar to the report of Zangaro et al. (2013). AM fungi are favoured in areas with more open exposure, and in a thin humus layer (Kauppinen et al. 2014); they are also favoured where there was higher light incidence and temperature, as in the report of Koide and Mosse (2004). Less vegetation cover and greater openness were observed in the crest area; and that could result in more lights and higher temperature. Quantitatively, the high levels of AM fungal spore densities and species richness in the crest soils could be related to favorable environmental conditions; higher AM fungal species richness and spore density therefore also appeared in the crest area.

Acaulospora morrowiae, A. scrobiculata and P. occultum produced higher amounts of spores (127–215/100 g soil) in the crest area. It is a benefit for these species to disseminate and colonize pioneer plants. Differences in the presence of P. occultum and S. nigra, and changes in the relative abundance of A. morrowiae andS. pellucida contributed to the differences in AM fungal communities between the two contrasting habitats. Previous studies have shown that vegetation types and environmental conditions such as soil pH, rainfall and soil type influence sporulation (Lovelock et al. 2003) and community structure (Goomaral et al. 2013) of AM fungi. Differences in vegetation result in changes in AM fungal communities.

Dynamics of the AM fungal community during the succession of vegetation recovery were recorded in this study. During the initial recovery stage (2001–2003) in the crest area, AM fungal species and their spore densities decreased from 8 to 3 species and 593 to 7 spores/100 g soil, respectively. At this stage, pioneer plant species including Sapium discolor, Mallotus paniculatus, Trema orientalis, Rhus chinensis var. roxburghii, Macaranga tanarius were often found on the crest of the hill. Acaulospora morrowiae, P. occultum, A. scrobiculata and A. tuberculata associated with these plants and produced high amounts of spores. These AM fungi contribute to soil aggregation (Rillig et al. 2010) and help plants to hold soil (Zhang et al. 2016).

Changes in abundance of specific AM fungal species might be caused by the absence or decrease of their host plants and increasing severity of environmental conditions. During this period, the dominant AM fungal species likely compete with other AM fungi or tolerate to the environmental stress (Chagnon et al. 2013). AM fungi of later successional stages often produced more soil hyphae than early successional species (Sikes et al. 2012). Responding to plant succession, changes in AM fungal community were observed in our study, including an absence of A. scrobiculata andA. tuberculata, a decrease in spore densities of A. morrowiae and P. occultum, and the presence of A. mellea, G. ambisporum, andG. deserticola. The composition of the AM fungal community varied greatly across different successional stages. Acaulospora scrobiculata, F. mosseae, and S. pellucida etc. were recorded at the earlier stage. Some species were only recovered in the later stage, such as G. ambisporum and G. deserticola. Community dynamics of AM fungi paralleled the dynamics of their host plant community. Following plant succession, AM fungal communities tend to switch from ruderal towards competitive life-history traits (Chagnon et al. 2013). Our results characterize the AM fungal diversity occurring during the trajectory of plant succession. This information would be helpful to enable the use of AM fungi as key drivers of successful restoration of degraded lands.

Ectomycorrhizal (EM) fungi have varied degrading enzymes (Plett and Martin 2011), which enable them to mobilize resources from a variety of mineral to organic substrates, including plant litter and coarse woody debris. Accompanied by plant canopy closure and increased accumulation of plant litter and soil humus, the incidence of EM fungi was recorded beginning in 2003. Amanita melleiceps was recorded until 2015. We first observed the appearance of AM fungi, then coexistence of AM and EM fungi. Dual mycorrhizal colonization has been recorded in many tree species (Toju et al. 2013). We also observed dual mycorrhizal colonization in roots of Pinus taiwanensis; the phenomenon might help plants to establish populations during succession.

Read (1993) suggested that dual-mycorrhizal-status plants might associate with AM fungi in early succession and then transition to association with EM fungi in late successional stages. Helm et al. (1996) found that EM plants and EM fungi appeared earlier in glacier succession because the spores of EM fungi are wind dispersed, while the spores of AM fungi are not. In primary succession such as glacier retreat, early-arriving fungal propagules are usually dispersed by wind. In this study, some AM propagules still remained in the habitat when the earthquake caused landslides and a huge loss of vegetation cover. In the other hand, Gehring et al. (2006) indicated that EM fungi preferred to colonize plant roots in moister environments and AM fungi colonized host in drier environments. After the earthquake, dry conditions in the study sites might be more appropriate for the colonization of AM fungi. We found that AM fungi arrived earlier than EM fungi during vegetation recovery after the earthquake. Our study provides field evidence that mycorrhizal fungal community changed after natural disturbance. The changes in AM fungal communities may mediate plant species turnover during succession.

References

  1. Allen EB, Chambers JC, Connor KF, Allen MF, Brown RW (1987) Natural reestablishment of mycorrhizae in disturbed alpine ecosystems. Arct Alp Res 19:11–20.

    Google Scholar 

  2. Allen MF, Crisafulli C, Friese CF, Jeakins SL (1992) Re-formation of mycorrhizal symbioses on mount St Helens, 1980–1990: interactions of rodents and mycorrhizal fungi. Mycol Res 96:447–453.

    Google Scholar 

  3. Asmelash F, Bekele T, Birhane E (2016) The potential role of arbuscular mycorrhizal fungi in the restoration of degraded lands. Front Microbiol 7:1095.

    PubMed  PubMed Central  Google Scholar 

  4. Attiwill PM (1994) The disturbance of forest ecosystems: the ecological basis for conservative management. For Ecol Manag 63:247–300.

    Google Scholar 

  5. Bellgard SE, Whelan RJ, Muston RM (1994) The impact of wildfire on vesicular-arbuscular mycorrhizal fungi and their potential to influence the re-establishment of post-fire plant communities. Mycorrhiza 4:139–146.

    Google Scholar 

  6. Chagnon PL, Bradley RL, Maherali H, Klironomos JN (2013) A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci 18:484–491

    CAS  PubMed  Google Scholar 

  7. Chen T-S (2005) Change detection for vegetation from landslides of the 921 earthquake at Mt. Jiujiufong with the NDVI analysis Journal of Endemic Species Research 7:63–75 (in Chinese)

    CAS  Google Scholar 

  8. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd ed. Plymouth, U.K.: PRIMER-E Ltd

  9. Dickie IA, Martínez-García LB, Koele N, Grelet GA, Tylianakis JM, Peltzer DA, Richardson SJ (2013) Mycorrhizas and mycorrhizal fungal communities throughout ecosystem development. Plant Soil 367:11–39.

    CAS  Google Scholar 

  10. García de León D, Moora M, Öpik M, Neuenkamp L, Gerz M, Jairus T, Vasar M, Bueno CG, Davison J, Zobel M (2016) Symbiont dynamics during ecosystem succession: co-occurring plant and arbuscular mycorrhizal fungal communities. FEMS Microbiol Ecol 92:fiw097.

    PubMed  Google Scholar 

  11. Gehring CA, Mueller RC, Whitham TG (2006) Environmental and genetic effects on the formation of ectomycorrhizal and arbuscular mycorrhizal associations in cottonwoods. Oecologia 149:158–164.

    PubMed  Google Scholar 

  12. Gerdemann JW, Nicolson TH (1963) Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Trans Br Mycol Soc 46:235–244.

    Google Scholar 

  13. Goomaral A, Undarmaa J, Matsumoto T, Yamato M (2013) Effect of plant species on communities of arbuscular mycorrhizal fungi in the Mongolian steppe. Mycoscience 54:362–367.

    Google Scholar 

  14. Grime JP, Mackey JML, Hillier SH, Read DJ (1987) Floristic diversity in a model system using experimental microcosms. Nature 328:420–422.

    Google Scholar 

  15. Helm DJ, Allen EB, Trappe JM (1996) Mycorrhizal chronosequence near Exit Glacier, Alaska. Can J Bot 74:1496–1506

    Google Scholar 

  16. Huang (2002) Monitoring and assessing the changes of vegetation cover at Jiujiufong nature reserve. Q J For Res 24:35–48

    CAS  Google Scholar 

  17. INVAM (2003) International culture collection of vesicular and arbuscular mycorrhizal fungi. Species description. Morgantown, West Virginia Agriculture and Forestry Experimental Station. Home page. http://invam.caf.wvu.edu. Accessed 31 Dec 2003

  18. Jenkins WR (1964) A rapid centrifugal-flotation technique for separating nematodes from soil. Plant Dis Rep 692

  19. Karandashov V, Nagy R, Wegmüller S, Amrhein N, Bucher M (2004) Evolutionary conservation of a phosphate transporter in the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 101:6285–6290.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Kauppinen M, Raveala K, Wäli PR, Ruotsalainen AL (2014) Contrasting preferences of arbuscular mycorrhizal and dark septate fungi colonizing boreal and subarctic Avenella flexuosa. Mycorrhiza 24:171–177.

    CAS  PubMed  Google Scholar 

  21. Kikvidze Z, Armas C, Fukuda K, Martínez-García LB, Miyata M, Oda-Tanaka A, Pugnaire FI, Wu B (2010) The role of arbuscular mycorrhizae in primary succession: differences and similarities across habitats. Web Ecol 10:50–57.

    Google Scholar 

  22. Klironomos JN, McCune J, Hart M, Neville J (2000) The influence of arbuscular mycorrhizae on the relationship between plant diversity and productivity. Ecol Lett 3:137–141.

    Google Scholar 

  23. Koide RT, Mosse B (2004) A history of research on arbuscular mycorrhiza. Mycorrhiza 14:145–163.

    PubMed  Google Scholar 

  24. Koziol L, Bever JD (2016) The missing link in grassland restoration: arbuscular mycorrhizal fungi inoculation increases plant diversity and accelerates succession. J Appl Ecol n/a-n/a 54:1301–1309.

    Google Scholar 

  25. Krüger C, Kohout P, Janoušková M, Püschel D, Frouz J, Rydlová J (2017) Plant communities rather than soil properties structure arbuscular mycorrhizal fungal communities along primary succession on a mine spoil. Front Microbiol 8.

  26. Lin TC, Wu CG (2007) Vesicular-arbuscular mycorrhizal fungi (VAMF) symbiotic with pioneer plants at Mt. Jiujiufong after the 921 earthquakes. Journal of Endemic Species Research 9:51–62 (in Chinese)

    Google Scholar 

  27. Lin W-T, Chou W-C, Lin C-Y, Huang P-H, Tsai J-S (2005) Vegetation recovery monitoring and assessment at landslides caused by earthquake in Central Taiwan. For Ecol Manag 210:55–66.

    Google Scholar 

  28. Lin G, McCormack ML, Guo D (2015) Arbuscular mycorrhizal fungal effects on plant competition and community structure. J Ecol 103:1224–1232.

    CAS  Google Scholar 

  29. Lovelock CE, Andersen K, Morton JB (2003) Arbuscular mycorrhizal communities in tropical forests are affected by host tree species and environment. Oecologia 135:268–279.

    PubMed  Google Scholar 

  30. Miransari M (2010) Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biol 12:563–569.

    CAS  PubMed  Google Scholar 

  31. Morton JB (1988) Taxonomy of VA mycorrhizal fungi: classification, nomenclature and identification. Mycotaxon 32:267–324

    Google Scholar 

  32. Neuenkamp L, Prober SM, Price JN, Zobel M, Standish RJ (2018) Benefits of mycorrhizal inoculation to ecological restoration depend on plant functional type, restoration context and time. Fungal Ecology (Accepted/In press):1–10.

  33. Oba H, Shinozaki N, Oyaizu H, Tawaraya K, Wagatsuma T, Barraquio WL, Saito M (2004) Arbuscular mycorrhizal fungal communities associated with some pioneer plants in the lahar area of Mt. Pinatubo, Philippines. Soil Sci Plant Nutr 50:1195–1203.

    Google Scholar 

  34. Oehl F, Alves a Silva G, Goto BT, Costa Maia L, Sieverding E (2011a) Glomeromycota: two new classes and a new order. Mycotaxon 116:365–379.

    Google Scholar 

  35. Oehl F, Sieverding E, Palenzuela J, Ineichen K (2011b) Advances in Glomeromycota taxonomy and classification. IMA Fungus Glob Mycol J 2:191–199.

    Google Scholar 

  36. Plett JM, Martin F (2011) Blurred boundaries: lifestyle lessons from ectomycorrhizal fungal genomes. Trends Genet 27:14–22.

    CAS  PubMed  Google Scholar 

  37. Read DJ (1993) Mycorrhiza in plant communities. Adv Plant Pathol 9:1–31

    Google Scholar 

  38. Rillig MC, Wright SF, Eviner VT (2002) The role of arbuscular mycorrhizal fungi and glomalin in soil aggregation: comparing effects of five plant species. Plant Soil 238:325–333

    CAS  Google Scholar 

  39. Rillig MC, Mardatin NF, Leifheit EF, Antunes PM (2010) Mycelium of arbuscular mycorrhizal fungi increases soil water repellency and is sufficient to maintain water-stable soil aggregates. Soil Biol Biochem 42:1189–1191.

    CAS  Google Scholar 

  40. Schenck NC, Pérez Y (1990) Manual for the identification of VA mycorrhizal fungi. Synergistic Publications, Gainesville, FL

    Google Scholar 

  41. Schüßler A, Walker C (2010) The Glomeromycota. A species list with new families and new genera. In: CreateSpace independent publishing platform. Gloucester, England

    Google Scholar 

  42. Sikes BA, Maherali H, Klironomos JN (2012) Arbuscular mycorrhizal fungal communities change among three stages of primary sand dune succession but do not alter plant growth. Oikos 121:1791–1800.

    Google Scholar 

  43. Smith SE, Read DJ (2010) Mycorrhizal Symbiosis. Academic Press

  44. Toju H, Yamamoto S, Sato H, Tanabe AS (2013) Sharing of diverse mycorrhizal and root-endophytic fungi among plant species in an oak-dominated cool–temperate forest. PLoS One 8:e78248.

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Turrini A, Sbrana C, Avio L, Njeru EM, Bocci G, Bàrberi P, Giovannetti M (2016) Changes in the composition of native root arbuscular mycorrhizal fungal communities during a short-term cover crop-maize succession. Biol Fertil Soils 52:643–653.

    Google Scholar 

  46. Vogelsang KM, Reynolds HL, Bever JD (2006) Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol 172:554–562.

    PubMed  Google Scholar 

  47. Wang Y, Huang J, Gao Y (2012) Arbuscular mycorrhizal colonization alters subcellular distribution and chemical forms of cadmium in Medicago sativa L. and resists cadmium toxicity. PLoS One 7:e48669.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Warner NJ, Allen MF, MacMahon JA (1987) Dispersal agents of vesicular-arbuscular mycorrhizal fungi in a disturbed arid ecosystem. Mycologia 79:721–730.

    Google Scholar 

  49. Wu B, Hogetsu T, Isobe K, Ishii R (2007) Community structure of arbuscular mycorrhizal fungi in a primary successional volcanic desert on the southeast slope of Mount Fuji. Mycorrhiza 17:495–506.

    CAS  PubMed  Google Scholar 

  50. Yang G, Liu N, Lu W, Wang S, Kan H, Zhang Y, Xu L, Chen Y (2014) The interaction between arbuscular mycorrhizal fungi and soil phosphorus availability influences plant community productivity and ecosystem stability. J Ecol 102:1072–1082.

    CAS  Google Scholar 

  51. Zangaro W, Rostirola LV, de Souza PB, de Almeida Alves R, Lescano LEAM, Rondina ABL, Nogueira MA, Carrenho R (2013) Root colonization and spore abundance of arbuscular mycorrhizal fungi in distinct successional stages from an Atlantic rainforest biome in southern Brazil. Mycorrhiza 23:221–233.

    PubMed  Google Scholar 

  52. Zhang H, Liu Z, Chen H, Tang M (2016) Symbiosis of arbuscular mycorrhizal fungi and Robinia pseudoacacia L. improves root tensile strength and soil aggregate stability. PLoS One 11:e0153378.

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

Financial support was provided by the Council of Agriculture, Executive Yuan, R. O. C. (Taiwan). We thank Dr. Chi-Guang Wu for assistance with identification of AM fungal spores. For assistance with field work, we thank Mr. E. L. Cheu and Ms. C. H. Wu.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Wan-Rou Lin.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Lin, T., Wang, P. & Lin, W. Changes of mycorrhizal fungal community occurring during the natural restoration after the chi-chi earthquake in Taiwan. Symbiosis 77, 177–184 (2019). https://doi.org/10.1007/s13199-018-0582-z

Download citation

Keywords

  • Earthquakes
  • Arbuscular mycorrhizal fungi
  • Pioneer species
  • Ectomycorrhizal fungi
  • In situ field study