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Ectomycorrhizal fungal communities in high mountain conifer forests in central Mexico and their potential use in the assisted migration of Abies religiosa

DOI:10.1007/s00572-018-0841-0
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Andrés Argüelles-Moyao
Andrés Argüelles-Moyao
Andrés Argüelles-Moyao
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Roberto Garibay-Orijel at Universidad Nacional Autónoma de México
Roberto Garibay-Orijel
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Abstract and Figures

Abies religiosa forests in central Mexico are the only overwinter refuge of the monarch butterfly and provide important ecosystem services. These forests have lost 55% of their original area and as a consequence, diversity and biotic interactions in these ecosystems are in risk. The aim of this study was to compare the soil fungal diversity and community structure in the Abies religiosa forests and surrounding Pinus montezumae, Pinus hartwegii, and coniferous mixed forest plant communities to provide data on ecology of mycorrhizal interactions for the assisted migration of A. religiosa. We sampled soil from five coniferous forests, extracted total soil DNA, and sequenced the ITS2 region by Illumina MiSeq. The soil fungi community was integrated by 1746 taxa with a species turnover ranging from 0.280 to 0.461 between sampling sites. In the whole community, the more abundant and frequent species were Russula sp. (aff. olivobrunnea), Mortierella sp.1, and Piloderma sp. (aff. olivacearum). The ectomycorrhizal fungi were the more frequent and abundant functional group. A total of 298 species (84 ectomycorrhizal) was shared in the five conifer forests; these widely distributed species were dominated by Russulaceae and Clavulinaceae. The fungal community composition was significantly influenced by altitude and the lowest species turnover happened between the two A. religiosa forests even though they have different soil types. As Pinus montezumae forests have a higher altitudinal distribution adjacent to A. religiosa and share the largest number of ectomycorrhizal fungi with it, we suggest these forests as a potential habitat for new A. religiosa populations.
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ORIGINAL ARTICLE
Ectomycorrhizal fungal communities in high mountain conifer forests
in central Mexico and their potential use in the assisted migration
of Abies religiosa
Andrés Argüelles-Moyao
1,2
&Roberto Garibay-Orijel
1
Received: 13 December 2017 /Accepted: 29 May 2018 /Published online: 11 June 2018
#Springer-Verlag GmbH Germany, part of Springer Nature 2018
Abstract
Abies religiosa forests in central Mexico are the only overwinter refuge of the monarch butterfly and provide important
ecosystem services. These forests have lost 55% of their original area and as a consequence, diversity and biotic
interactions in these ecosystems are in risk. The aim of this study was to compare the soil fungal diversity and
community structure in the Abies religiosa forests and surrounding Pinus montezumae,Pinus hartwegii,andconiferous
mixed forest plant communities to provide data on ecology of mycorrhizal interactions for the assisted migration of A.
religiosa. We sampled soil from five coniferous forests, extracted total soil DNA, and sequenced the ITS2 region by
Illumina MiSeq. The soil fungi community was integrated by 1746 taxa with a species turnover ranging from 0.280 to
0.461 between sampling sites. In the whole community, the more abundant and frequent species were Russula sp. (aff.
olivobrunnea), Mortierella sp.1, and Piloderma sp. (aff. olivacearum). The ectomycorrhizal fungi were the more fre-
quent and abundant functional group. A total of 298 species (84 ectomycorrhizal) was shared in the five conifer forests;
these widely distributed species were dominated by Russulaceae and Clavulinaceae. The fungal community composition
was significantly influenced by altitude and the lowest species turnover happened between the two A. religiosa forests
even though they have different soil types. As Pinus montezumae forests have a higher altitudinal distribution adjacent
to A. religiosa and share the largest number of ectomycorrhizal fungi with it, we suggest these forests as a potential
habitat for new A. religiosa populations.
Keywords Fungal ecology .Beta diversity .Functional groups .Environmental decision-making .Monarch butterfly habitat
Introduction
The high species extinction rate in the Anthropocene (Pievani
2014) is driving to a dramatic loss of lineages constraining the
functionality of ecosystems and reducing our ability to adapt
to a changing environment. In Mexico, the area of primary
temperate forest has been reduced substantially over the pre-
vious 20 years. This has been particularly severe for Pinus and
Quercus species (Miranda-Aragón et al. 2012) and for Abies
religiosa (Ramirez et al. 2015). High altitude conifer forests
are among the most imperiled ecosystems in the Trans-
Mexican Volcanic Belt in central Mexico due to climate
change and deforestation. Temperate forests in these moun-
tains are characterized by an alpine monodominant Pinus
hartwegii forest at elevations above 3500 m, followed by
Pinus montezumae from 3000 to 3500 m and A. religiosa from
2800 to 3000 m.
Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s00572-018-0841-0) contains supplementary
material, which is available to authorized users.
*Roberto Garibay-Orijel
rgaribay@ib.unam.mx
Andrés Argüelles-Moyao
evoandres@gmail.com
1
Laboratorio de Sistemática, Ecología y Aprovechamiento de Hongos
Ectomicorrízicos, Departamento de Botánica, Instituto de Biología,
Universidad Nacional Autónoma de México, Circuito Exterior s/n,
Ciudad Universitaria. Del. Coyoacán, C.P. 04510 Mexico
City, CDMX, Mexico
2
Posgrado en Ciencias Biológicas, Edificio B, 1° Piso, Unidad de
Posgrado, Circuito de Posgrados, Universidad Nacional Autónoma
de México, Ciudad Universitaria, Del. Coyoacán, C.P. 04510 Mexico
City, CDMX, Mexico
Mycorrhiza (2018) 28:509–521
https://doi.org/10.1007/s00572-018-0841-0
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... This forest has a diverse understory while the overstory is dominated by Abies religiosa. Nonetheless, other ectomycorrhizal hosts are also present but in very low abundance, such as Alnus jorullensis, Salix paradoxa, Comarostaphyllis discolor, Quercus laurifolia (scarce), and Arbutus xalapensis (Argüelles-Moyao et al., 2017;Argüelles-Moyao and Garibay-Orijel, 2018). ...
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Abies religiosa's forests are severely endangered as a result of climate change; to save this species and its biological interactions, population assisted migration is discussed in forest management, but not in the microbial ecology field. Our objectives were to analyze its mycorrhizal networks; and, with this data, to identify potential facilitator plants and it's most important mycorrhizal fungal links. This information could be used together in assisted migration programs to connect Abies religiosa saplings to their mycorrhizal network and improve their field establishment. We collected 47 rhizosphere samples from 19 plant species and sequenced their fungal ITS2 region by Illumina. In the whole fungal community, 464 species were mycorrhizal fungi with assigned guild (32%). In this subset, 85 fungi are arbuscular, 365 ectomycorrhizal and 14 from orchid-mycorriza. The Abies religiosa bipartite network is low nested and highly modular, and has a scale-free architecture. Besides Abies religiosa, the plants with the largest degree and the lowest average shortest path were Salix paradoxa, Muhlenbergia spp., and Baccharis conferta. The most important fungal nodes are species of Cortinarius, Genea, Rhodoscypha, Russula, and Tomentella. We suggest to evaluate the Abies' future establishment in the following scheme: in the first year reintroduce Muhlenbergia spp., and Baccharis conferta, in the second year Salix paradoxa, and in the third year–once the mycorrhizal network is reestablished– Abies religiosa' saplings in close proximity of these plants. This scheme is proposed using the data and network analyses of the present study. Authorized share link: https://authors.elsevier.com/a/1evxY,XbFFXEDn
... The genus typically associates with arbuscular mycorrhizal (AM) fungi (Soudzilovskaia et al., 2020) although some studies have reported individuals forming ECM associations (Reinsvold and Reeves, 1986;Dean et al., 2015). Juniperus species have been largely re-introduced for reforesting pine-oak forests of Central Mexico that are naturally dominated by ECM associations (García-Guzmán et al., 2017;Argüelles-Moyao and Garibay-Orijel, 2018). Co-occurring AM and ECM plants are likely to spontaneously share mycorrhizal fungi in their native range (Kadowaki et al., 2018;Toju and Sato, 2018), but these aspects have scarcely been addressed for reforestation purposes. ...
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... To date Faxon fir has not been investigated for its reliance on mycorrhizal symbioses in environmental adaptation and stress tolerance, though some recent studies suggested that the responses of Faxon fir to warming might involve alteration of nutrient uptakes by ECM roots (Pu et al., 2017;Lu et al., 2017). In Abies firma, it was found that ECM morphology identification and DNA sequence greatly varied under different environmental gradients (Matsuda and Hijii,1999a, 1999b, 2004; whereas the study of Argüelles-Moyao and Garibay-Orijel (2018) showes that ECM symbioses determine the habitat range of Abies religiosa in high elevational distribution. ...
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Full-text available
  • Jan 2018
Ectomycorrhizal (ECM) and ectendomycorrhizal fungal species associated with Pinus montezumae were recorded in 8 year-old trees established in microcosms and compared with those associated with 2 year-old trees, in order to determine their persistence over the long-term. Mycorrhizal root tips were morphologically and anatomically characterized and sequenced. The extension of extramatrical mycelium of ECM fungi with long exploration strategies was evaluated. In total, 11 mycorrhizal species were registered. Seven mycorrhizal species were detected on both 2 and 8 year-old pines: Atheliaceae sp., Rhizopogon aff. fallax, R. aff. occidentalis, Suillus pseudobrevipes, Tuber separans, Wilcoxina mikolae and Wilcoxina rehmii. One species, Thelephora terrestris, was exclusively associated with two year–old seedlings, while Cenococcum geophilum, Pezizaceae sp. and Pyrenomataceae sp. were exclusively found on 8 year-old trees. Atheliaceae sp. was the ECM fungal species that presented the most abundant mycelium. Finally, we report one new fungal species of Pezizaceae occurring as a symbiont of P. montezumae.
Ectomycorrhizal pre-inoculation of Pinus hartwegii and Abies religiosa is replaced by native fungi in a temperate forest of central Mexico
Article
Full-text available
  • Feb 2018
http://rdcu.be/uhpb Few studies have focused on analyzing the effect of native inoculated ectomycorrhizal (ECM) fungal strains on seedlings under field conditions in temperate forests. However, it is crucial to verify that the positive effects of ECM under nursery conditions also occur in the field, favoring their performance. We evaluated the short-term effect of ECMonthree-year-old seedlings of Pinus hartwegii and Abies religiosa in central Mexico by subjecting them to four treatments: inoculation with Inocybe splendens, inoculation with Suillus brevipes (both native strains), inoculation with forest soil, and non-inoculated plants. Percentage of ECM colonization, plant growth (shoot height and stem diameter),and physiological (osmotic potential, stomatal conductance, CO2 assimilation and wáter use efficiency) responses were evaluated. We found that these two ECM species were partial (P. hartwegii) or totally (A. religiosa) replaced after one and a half years in the field. P. hartwegii seedlings increased their water use efficiency during the dry season, but in A. religiosa seedlings, a clear strategy for avoiding water stress was not detected. This ECM replacement had a negative effect on the physiological performance of A. religiosa. Our results emphasize the importance of selecting compatible fungal-host species combinations for nursery inoculation and of using sources of inoculum adapted to the environmental conditions of the transplant site, ensuring root colonization prior to field transplanting to minimize seedling mortality due to wáter stress.
R: A Language and Environment for Statistical Computing
Book
  • Jan 2015
R: A Language and Environment for Statistical Computing
Book
  • Jan 2017
Global Biogeography and Invasions of Ectomycorrhizal Plants: Past, Present and Future
Chapter
  • Jun 2017
Ectomycorrhizal (EcM) plants have evolved multiple times from arbuscular mycorrhizal or non-mycorrhizal ancestors, and they have a broad distribution on Earth, with abundant recent human introductions. The evolution as well as historical and current distribution of these EcM plant groups and mechanisms of their invasion have remained poorly understood. The purpose of this review/synthesis is fivefold: (1) to determine the time and place of evolution for EcM plant groups based on dated phylogenies and fossil evidence, (2) to characterise the historical and current natural distribution patterns based on fossil record and information from accumulated observations and specimens, (3) to establish the major global biodiversity hotspots for EcM plants based on the present distribution patterns of EcM plant lineages, (4) to determine the relative importance and role of EcM plants in human-mediated plant invasions and to shed light on the mechanisms and (5) integrate this information with climate change scenarios into predictions of the future biogeography of EcM plants.