Surviving after an eruption: Ecosystem dynamics and mycorrhizae in Nothofagus pumilio forests affected by the 2011 Puyehue Cordón-Caulle tephra

https://doi.org/10.1016/j.foreco.2020.118535Get rights and content

Highlights

  • Sites with tephra had N. pumilio regeneration and low understory plant richness.

  • Nothofagus pumilio seedlings in the tephra had ectomycorrhizal fungi (EM).

  • Differences in plant growth and EM behavior were observed between sites.

  • The composition of EM communities in the tephra was different from that in forest soil.

  • EM are an effective adaptation mechanism for stressful, post-eruption conditions.

Abstract

Volcanic eruptions affect ecosystems drastically, and ectomycorrhizal fungi (EM) may play a critical role in forest regeneration. Nothofagus species are usually ectomycorrhizal. The 2011 Puyehue Cordón-Caulle volcanic complex (PCCVC) eruption covered vast areas of N. pumilio forests with thick tephra deposits. The main objectives of this work were to characterize the forest environment following tephra deposition, and to analyze the natural regeneration and development of N. pumilio and associated EM communities. Three study sites were selected and sampled two and three years after the PCCVC eruption. Two sites had a thick tephra layer (50 cm); in one of them most of the tree layer was dead (Highly Affected-Tephra) whereas in the other, most of the adult trees were alive (Affected-Tephra). The third site had minimal tephra deposition (Non-Affected). Physicochemical properties of the substrate, biological environmental factors and EM behavior of N. pumilio seedlings and adults were evaluated in all three sites. The physicochemical properties of the substrate and environmental characteristics differed among sites. Both seedlings and adults had EM in all three sites. The frequency of six-month-old seedlings with EM (40%) and their colonization values (<12%) were significantly lower in both tephra-affected sites than in the Non-affected site (100% and 80 %, respectively). However, all the 18-month-old seedlings from the tephra-affected sites had EM and their colonization increased almost to the value of the seedlings from the Non-Affected site. In both tephra-affected sites N. pumilio seedlings were associated with some exclusive fungal species, which could have a primary successional role. The early, increasing EM colonization recorded in seedlings after the eruption supports the idea of the strong dependence of Nothofagus trees on this symbioses, and highlights that this mutualism could be an effective adaptive mechanism under stressful conditions. Our findings also suggest that EM symbiosis in N. pumilio persists even after a severe disturbance and is regulated by several factors such as time after eruption, availability and type of mycorrhizal inoculum, plant development and physicochemical substrate composition.

Introduction

Major volcanic eruptions are catastrophic events which affect ecosystems drastically due to the ejection and emission of gases, tephra, pumice and lava. These sudden processes can significantly alter landscape structure and the population dynamics of many species (Dale et al., 2005, Moore et al., 2008, González et al., 2014, Fernández et al., 2018, Moguilevsky et al., 2018). Among the most widespread disturbances associated with volcanic activity are tephra fall and deposition (del Moral and Grishin, 1999). Tephra and other pyroclastic materials can be transported great distances and affect thousands of square kilometers (Dale et al., 2005), modifying plant growth and productivity (Lawrence, 2005, Ghermandi et al., 2015, Magnin et al., 2016, Moguilevsky et al., 2018).

Although plant establishment depends on many factors, such as the physicochemical characteristics of tephra deposits and light incidence (Allen et al., 2005, Antos and Zobel, 2005, Moguilevsky et al., 2018), pioneer woody plants are able to become established shortly after tephra deposition (Antos and Zobel, 2005, Obase et al., 2007, Grosfeld and Puntieri, 2013, González et al., 2014, Ferreiro et al., 2018). In thick tephra deposits (over 50 cm deep) the entire understory can be buried, thus retarding the natural regeneration of the vegetation cover. In addition, superficial fine-particle tephra (<63 µm) can form a cement-like layer, hindering plant establishment (González et al., 2014). Biotic factors, such as the type and composition of the pre-existing plant community (Crisafulli et al., 2005, Ferreiro et al., 2018), dominant tree species (González et al., 2014, Magnin et al., 2016) and soil microbial communities (Halvorson et al., 2005, Fernández et al., 2018) must also be considered when assessing post-eruption vegetation changes.

Soil microorganisms are considered relevant components of ecosystems due to their influence on key ecosystem processes, including plant nutrient acquisition (Smith and Read, 2008), biogeochemical cycling (Tiedje, 1988, Kowalchuk and Stephen, 2001, Hogberg et al., 2001) and soil formation (Rillig and Mummey, 2006). Ectomycorrhizal fungi (EM) form symbiotic relationships with woody plants, which are benefited in terms of water and nutrient uptake, in addition to other improvements provided by this symbiosis (Dighton et al., 2005, Smith and Read, 2008). Due to their multiple effects on the host plant, EM have a strong influence on the establishment and growth of many tree species, and contribute to the aboveground biodiversity and to plant productivity (van der Heijden et al., 2008). In fact, many authors have highlighted the contribution of EM fungi in the recovery of forests after major disturbances (Perry et al., 1987, Dunabeitia et al., 2004, Quoreshi et al., 2008, Smith and Read, 2008), and in plant succession (Allen et al., 2005). Consequently, EM probably played critical roles in the growth and survival of their host plants after volcanic eruptions, and strongly influenced the natural regeneration of forests (Allen et al., 1992, Allen et al., 1995, Cázares et al., 2005, Nara, 2005, Nara et al., 2003, Vogel, 1996). The successful establishment of EM in plants at primary successional sites can be hindered, especially in severely devastated volcanic deserts (Allen et al., 1992).

In June 2011 a large eruption took place in the Puyehue Cordón Caulle volcanic complex (PCCVC), located in the Chilean southern Andes (Los Lagos region). This eruption released more than 950 million tons of tephra that covered an area of 240,000 km2 along a west-to-east gradient in Argentina (Gaitán et al., 2011). Several regions were affected by tephra deposition, including steppe and forest ecosystems (Puntieri et al., 2013, González et al., 2014, Ghermandi et al., 2015, Magnin et al., 2016, Edwards et al., 2017). Among the most severely affected forests were those dominated by Nothofagus pumilio (Poepp. and Endl.) Krasser (lenga; González et al., 2014), where massive tree deaths occurred (Puntieri et al., 2013, Magnin et al., 2016). Nothofagus pumilio forests occupy a large distribution range in high Andean environments of northwestern Patagonia (González et al., 2006). These forests are important not only from an ecological perspective, but also economically, as the quality wood they produce is highly appreciated in national and international forestry markets (Bava and Rechene, 2004, González et al., 2006). In Patagonia, Nothofagus species are extensively colonized by EM, with usually high colonization rates (>70%; Diehl et al., 2003, Diehl et al., 2008, Longo et al., 2011, Fernández et al., 2015), like other Nothofagus around the world (Orlovich and Cairney, 2004, Tedersoo et al., 2009).

The PCCVC eruption represented a unique opportunity to study forest regeneration strategies and the role of EM symbioses at the earliest stages of plant community recovery from a major disturbance. A recent study on sites affected by the PCCVC eruption has shown that N. pumilio seedlings are able to grow on tephra, and that their growth in that substrate is influenced by available P and light incidence (Moguilevsky et al., 2018); soil fungal communities, particularly Basidiomycetes, and total fungi were found to be affected by substrate type, light intensity, presence of understory plants, mycelial networks, and seedling size (Fernández et al., 2018). These studies suggested that the EM present in the seedling roots constituted one of the most important factors determining rhizosphere Basidiomycete communities.

The aim of this work was to characterize the forest environment following tephra deposition, and to analyze the natural regeneration and development of N. pumilio and their associated EM in the first two growing seasons after the PCCVC eruption. Abiotic and biotic factors, including the growth of N. pumilio seedlings and EM behavior, were assessed in three N. pumilio forests that were affected differently by the eruption.

Section snippets

Study area

The PCCVC eruption occurred in June 2011. This study was conducted in 2013 and 2014 in three native monospecific N. pumilio forests located within the Nahuel Huapi National Park (NHNP, northwestern Patagonia, Argentina; Fig. 1). The climate in this region is influenced by the Andean cordillera, which forms a barrier to the wet westerly winds from the Pacific Ocean. Precipitation ranges from 3000 mm year−1 on the western side of the NHNP to 700 mm year−1 in the east (Conti, 1998). Winters are

Forest characterization

Light incidence and percentage of dead N. pumilio trees were high, intermediate and low for HA-T, A-T and NA sites, respectively (Table 1). Tree density varied between 933 and 2888 trees ha−1, and DBH between 6.4 and 47.8 cm, with differences between sites not significant (p = 0.147 and p = 0.390, respectively; Table 1). Nothofagus pumilio seedling regeneration was significantly higher (p < 0.001) in A-T (1598 seedlings) than in the other two sites (335 and 213 seedlings in HA-T and NA,

Discussion

Sites affected by volcanic eruptions usually have different combinations of tephra deposition frequency, depth and texture, resulting in a wide range of plant responses (Antos and Zobel, 2005, Swanson et al., 2016). This was observed in Patagonia after the 2011 PCCVC eruption. At Cerro Otto (NA site), 70 km eastwards from the PCCVC, the tephra deposit was null or very thin (<1 cm) and there was no tree or understory vegetation death. In both sites located nearer to the PCCVC the tephra deposit

Conclusions

The PCCVC eruption modified forest structure and dynamics by affecting the understory vegetation, the survival and regeneration of the dominant tree species, N. pumilio, and the relationships between this species and EM fungal communities. The effects of the eruption on the vegetation depended on factors other than distance from the volcano, such as tephra thickness and physicochemical characteristics, light incidence and plant-plant competition. Some plant species, native to regions with a

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

We are grateful to Mr. Jorge Puga and Lic. Pablo Albear for collaborating in the sampling, to Lic. Ayelen Carron and Dr. Marina Stecconi for their academic collaboration and to Audrey Urquhart for language revision. We also thank National Park Administration for giving us permission to work in a protected area (Permission N° 1280/17). Financial support for this work was provided by grants: B200 (Universidad Nacional del Comahue), PICT2018-4029 (FONCyT, Fondo para la Investigación Científica y

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