Local abiotic conditions are more important than landscape context for structuring arbuscular mycorrhizal fungal communities in the roots of a forest herb

Boeraeve, Margaux; Honnay, Olivier; Jacquemyn, Hans

doi:10.1007/s00442-019-04406-z

Plant-microbe-animal interactions – original research
Published: 11 May 2019

Local abiotic conditions are more important than landscape context for structuring arbuscular mycorrhizal fungal communities in the roots of a forest herb

Oecologia volume 190, pages 149–157 (2019)Cite this article

592 Accesses
11 Citations
2 Altmetric
Metrics details

Abstract

Due to human influence, large tracts of natural vegetation have been cleared and replaced by other types of land use, resulting in highly fragmented landscapes consisting of small fragments of well-conserved habitat scattered within a matrix of intensively managed land. Changes in land use and associated fragmentation have important consequences for biodiversity in the remaining fragments. Most studies so far have investigated the impact of land use change on macro-organisms, but little is known about how landscape fragmentation affects microbial communities. Here, we studied how changes in land use and abiotic conditions affected the arbuscular mycorrhizal fungal (AMF) communities in the roots of the forest herb Stachys sylvatica. Root samples were collected from 40 populations occurring in fragmented forest patches of varying age and size embedded within an agricultural landscape. Our results showed that forest age and isolation did not affect AMF diversity or community composition, suggesting that AMF disperse easily throughout the landscape and that AMF communities reassemble fast in recently established forest patches. On the other hand, AMF richness increased with increasing forest area, indicating that small forest sizes limit AMF richness. Additionally, AMF richness increased with increasing soil pH and decreased with soil nitrate content, while AMF community composition was affected plant-available phosphorus. Overall, these results show that landscape context is less important than local abiotic conditions for structuring AMF communities. However, the significant area effect indicates that further reductions in forest area will lead to impoverished AMF communities, potentially affecting long-term plant fitness and community structure.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

Bainard LD, Bainard JD, Hamel C, Gan Y (2014) Spatial and temporal structuring of arbuscular mycorrhizal communities is differentially influenced by abiotic factors and host crop in a semi-arid prairie agroecosystem. FEMS Microbiol Ecol 88:333–344. https://doi.org/10.1111/1574-6941.12300
Article CAS PubMed Google Scholar
Bender SF, Conen F, van der Heijden MGA (2015) Mycorrhizal effects on nutrient cycling, nutrient leaching and N₂O production in experimental grassland. Soil Biol Biochem 80:283–292. https://doi.org/10.1016/j.soilbio.2014.10.016
Article CAS Google Scholar
Borcard D, Legendre P (2012) Is the Mantel correlogram powerful enough to be useful in ecological analysis? A simulation study. Ecology 93:1473–1481. https://doi.org/10.1890/11-1737.1
Article PubMed Google Scholar
Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77. https://doi.org/10.1007/s11104-008-9877-9
Article CAS Google Scholar
Butaye J, Jacquemyn H, Honnay O, Hermy M (2001) The species pool concept applied to forests in a fragmented landscape: dispersal limitation versus habitat limitation. J Veg Sci 13:27–34
Article Google Scholar
Camenzind T, Hempel S, Homeier J, Horn S, Velescu A, Wilcke W, Rillig MC (2014) Nitrogen and phosphorus additions impact arbuscular mycorrhizal abundance and molecular diversity in a tropical montane forest. Glob Chang Biol 20:3646–3659. https://doi.org/10.1111/gcb.12618
Article Google Scholar
Carrino-Kyker SR, Kluber LA, Petersen SM, Coyle KP, Hewins CR, DeForest JL, Smemo KA, Burke DJ (2016) Mycorrhizal fungal communities respond to experimental elevation of soil pH and P availability in temperate hardwood forests. FEMS Microbiol Ecol 92:fiw024. https://doi.org/10.1093/femsec/fiw024
Article CAS PubMed Google Scholar
Chagnon P-L, Bradley RL, Maherali H, Klironomos JN (2013) A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci 18:484–491. https://doi.org/10.1016/j.tplants.2013.05.001
Article CAS PubMed Google Scholar
Crouzeilles R, Curran M, Ferreira MS, Lindenmayer DB, Grelle CEV, Rey Benayas JM (2016) A global meta-analysis on the ecological drivers of forest restoration success. Communication, Nat. https://doi.org/10.1038/ncomms11666
Book Google Scholar
de León DG, Moora M, Öpik M, Jairus T, Neuenkamp L, Vasar M, Bueno CG, Gerz M, Davison J, Zobel M (2016a) Dispersal of arbuscular mycorrhizal fungi and plants during succession. Acta Oecol 77:128–135. https://doi.org/10.1016/j.actao.2016.10.006
Article Google Scholar
de León DG, Moora M, Öpik M, Neuenkamp L, Gerz M, Jairus T, Vasar M, Bueno CG, Davison J, Zobel M (2016b) Symbiont dynamics during ecosystem succession: co-occurring plant and arbuscular mycorrhizal fungal communities. FEMS Microbiol Ecol 92:fiw097. https://doi.org/10.1093/femsec/fiw097
Article CAS Google Scholar
De Smedt P, Baeten L, Proesmans W, Berg MP, Brunet J, Cousins SAO, Decocq G, Deconchat M, Diekmann M, Gallet-Moron E, Giffard B, Liira J, Martin L, Ooms A, Valdés A, Wulf M, Hermy M, Bonte D, Verheyen K (2018) Linking macrodetritivore distribution to desiccation resistance in small forest fragments embedded in agricultural landscapes in Europe. Landsc Ecol 33:407–421. https://doi.org/10.1007/s10980-017-0607-7
Article Google Scholar
Dekeukeleire D, Janssen R, Haarsma A-J, Bosch T, van Schaik J (2016) Swarming behaviour, catchment area and seasonal movement patterns of the Bechstein’s bat: implications for conservation. Acta Chiropterol. https://doi.org/10.3161/15081109ACC2016.18.2.004
Article Google Scholar
Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH (2009) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4:337. https://doi.org/10.1038/ismej.2009.122
Article PubMed Google Scholar
Dumbrell AJ, Ashton PD, Aziz N, Feng G, Nelson M, Dytham C, Fitter AH, Helgason T (2011) Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing. New Phytol 190:794–804. https://doi.org/10.1111/j.1469-8137.2010.03636.x
Article CAS Google Scholar
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996. https://doi.org/10.1038/nmeth.2604
Article CAS PubMed Google Scholar
Egerton-Warburton LM, Johnson NC, Allen EB (2007) Mycorrhizal community dynamics following nitrogen fertilization: a cross-site test in five grasslands. Ecol Monogr 77:527–544. https://doi.org/10.1890/06-1772.1
Article Google Scholar
Entry JA, Rygiewicz PT, Watrud LS, Donnelly PK (2002) Influence of adverse soil conditions on the formation and function of Arbuscular mycorrhizas. Adv Environ Res 7:123–138. https://doi.org/10.1016/S1093-0191(01)00109-5
Article CAS Google Scholar
Fischer J, Lindenmayer DB (2007) Landscape modification and habitat fragmentation: a synthesis. Glob Ecol Biogeogr 16:265–280. https://doi.org/10.1111/j.1466-8238.2007.00287.x
Article Google Scholar
Grilli G, Urcelay C, Galetto L (2012) Forest fragment size and nutrient availability: complex responses of mycorrhizal fungi in native–exotic hosts. Plant Ecol 213:155–165. https://doi.org/10.1007/s11258-011-9966-3
Article Google Scholar
Grilli G, Urcelay C, Galetto L, Davison J, Vasar M, Saks Ü, Jairus T, Öpik M (2015) The composition of arbuscular mycorrhizal fungal communities in the roots of a ruderal forb is not related to the forest fragmentation process. Environ Microbiol 17:2709–2720. https://doi.org/10.1111/1462-2920.12623
Article PubMed Google Scholar
Grilli G, Longo S, Huais PY, Pereyra M, Verga EG, Urcelay C, Galetto L (2017) Fungal diversity at fragmented landscapes: synthesis and future perspectives. Curr Opin Microbiol 37:161–165. https://doi.org/10.1016/j.mib.2017.09.003
Article CAS PubMed Google Scholar
Haddad NM, Brudvig LA, Clobert J, Davies KF, Gonzalez A, Holt RD, Lovejoy TE, Sexton JO, Austin MP, Collins CD, Cook WM, Damschen EI, Ewers RM, Foster BL, Jenkins CN, King AJ, Laurance WF, Levey DJ, Margules CR, Melbourne BA, Nicholls AO, Orrock JL, Song D-X, Townshend JR (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv. https://doi.org/10.1126/sciadv.1500052
Article PubMed PubMed Central Google Scholar
Hill MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54:427–432. https://doi.org/10.2307/1934352
Article Google Scholar
Honnay O, Hermy M, Coppin P (1999) Impact of habitat quality on forest plant species colonization. For Ecol Manag 115:157–170. https://doi.org/10.1016/S0378-1127(98)00396-X
Article Google Scholar
Honnay O, Helsen K, Van Geel M (2017) Plant community reassembly on restored semi-natural grasslands lags behind the assembly of the arbuscular mycorrhizal fungal communities. Biol Conserv 212:196–208. https://doi.org/10.1016/j.biocon.2017.06.017
Article Google Scholar
Jacquemyn H, Butaye J, Hermy M (2001) Forest plant species richness in small, fragmented mixed deciduous forest patches: the role of area, time and dispersal limitation. J Biogeogr 28:801–812. https://doi.org/10.1046/j.1365-2699.2001.00590.x
Article Google Scholar
Jacquemyn H, Butaye J, Hermy M (2003) Influence of environmental and spatial variables on regional distribution of forest plant species in a fragmented and changing landscape. Ecography (Cop.) 26:768–776. https://doi.org/10.1111/j.0906-7590.2003.03620.x
Article Google Scholar
Johnson D, Vandenkoornhuyse PJ, Leake JR, Gilbert L, Booth RE, Grime JP, Young JPW, Read DJ (2004) Plant communities affect arbuscular mycorrhizal fungal diversity and community composition in grassland microcosms. New Phytol 161:503–515. https://doi.org/10.1046/j.1469-8137.2003.00938.x
Article Google Scholar
Kawahara A, An G-H, Miyakawa S, Sonoda J, Ezawa T (2016) Nestedness in arbuscular mycorrhizal fungal communities along soil pH gradients in early primary succession: acid-tolerant fungi are pH generalists. PLoS One 11:1–20. https://doi.org/10.1371/journal.pone.0165035
CAS Article Google Scholar
Konvalinková T, Jansa J (2016) Lights off for arbuscular mycorrhiza: on its symbiotic functioning under light deprivation. Front Plant Sci 7:782. https://doi.org/10.3389/fpls.2016.00782
Article PubMed PubMed Central Google Scholar
Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq illumina sequencing platform. Appl Environ Microbiol 79:5112–5120. https://doi.org/10.1128/AEM.01043-13
Article CAS PubMed PubMed Central Google Scholar
Larimer AL, Bever JD, Clay K (2012) Consequences of simultaneous interactions of fungal endophytes and arbuscular mycorrhizal fungi with a shared host grass. Oikos 121:2090–2096. https://doi.org/10.1111/j.1600-0706.2012.20153.x
Article Google Scholar
Liu Y, Johnson NC, Mao L, Shi G, Jiang S, Ma X, Du G, An L, Feng H (2015) Phylogenetic structure of arbuscular mycorrhizal community shifts in response to increasing soil fertility. Soil Biol Biochem 89:196–205. https://doi.org/10.1016/j.soilbio.2015.07.007
Article CAS Google Scholar
López-García Á, Azcón-Aguilar C, Barea JM (2014) The interactions between plant life form and fungal traits of arbuscular mycorrhizal fungi determine the symbiotic community. Oecologia 176:1075–1086. https://doi.org/10.1007/s00442-014-3091-7
Article PubMed Google Scholar
López-García Á, Varela-Cervero S, Vasar M, Öpik M, Barea JM, Azcón-Aguilar C (2017) Plant traits determine the phylogenetic structure of arbuscular mycorrhizal fungal communities. Mol Ecol 26:6948–6959. https://doi.org/10.1111/mec.14403
Article PubMed Google Scholar
Mangan SA, Adler GH (2000) Consumption of arbuscular mycorrhizal fungi by terrestrial and arboreal small mammels in a Panamanian cloud forest. J Mammal 81:563–570. https://doi.org/10.1644/1545-1542(2000)081%3c0563:COAMFB%3e2.0.CO;2
Article Google Scholar
Naaf T, Kolk J (2015) Colonization credit of post-agricultural forest patches in NE Germany remains 130–230 years after reforestation. Biol Conserv 182:155–163. https://doi.org/10.1016/j.biocon.2014.12.002
Article Google Scholar
Nilsson RH, Anslan S, Bahram M, Wurzbacher C, Baldrian P, Tedersoo L (2019) Mycobiome diversity: high-throughput sequencing and identification of fungi. Nat Rev Microbiol 17:95–109. https://doi.org/10.1038/s41579-018-0116-y
Article CAS PubMed Google Scholar
Oksanen J, Blanchet FG, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Szoecs E, Wagner H (2016) Vegan: community ecology package
Olsen SR (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. US Dept. of Agriculture, Washington
Google Scholar
Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij JM, Reier Ü, Zobel M (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188:223–241. https://doi.org/10.1111/j.1469-8137.2010.03334.x
Article CAS PubMed Google Scholar
Peay KG, Bruns TD, Kennedy PG, Bergemann SE, Garbelotto M (2007) A strong species–area relationship for eukaryotic soil microbes: island size matters for ectomycorrhizal fungi. Ecol Lett 10:470–480. https://doi.org/10.1111/j.1461-0248.2007.01035.x
Article PubMed Google Scholar
QGIS Development Team (2009) QGIS geographic information system. Open Source Geospatial Foundation Project. http://qgis.osgeo.org
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
Sikes BA, Maherali H, Klironomos JN (2014) Mycorrhizal fungal growth responds to soil characteristics, but not host plant identity, during a primary lacustrine dune succession. Mycorrhiza 24:219–226. https://doi.org/10.1007/s00572-013-0531-x
Article PubMed Google Scholar
Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, Bonito G, Corradi N, Grigoriev I, Gryganskyi A, James TY, O’Donnell K, Roberson RW, Taylor TN, Uehling J, Vilgalys R, White MM, Stajich JE (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–1046. https://doi.org/10.3852/16-042
Article CAS PubMed PubMed Central Google Scholar
Van Aarle IM, Olsson PA, Söderström B (2002) Arbuscular mycorrhizal fungi respond to the substrate pH of their extraradical mycelium by altered growth and root colonization. New Phytol 155:173–182. https://doi.org/10.1046/j.1469-8137.2002.00439.x
Article Google Scholar
van der Heijden MGA, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310. https://doi.org/10.1111/j.1461-0248.2007.01139.x
Article PubMed Google Scholar
van der Heijden MGA, Martin FM, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423. https://doi.org/10.1111/nph.13288
Article CAS PubMed Google Scholar
Van Geel M, Busschaert P, Honnay O, Lievens B (2014) Evaluation of six primer pairs targeting the nuclear rRNA operon for characterization of arbuscular mycorrhizal fungal (AMF) communities using 454 pyrosequencing. J Microbiol Methods 106:93–100. https://doi.org/10.1016/j.mimet.2014.08.006
Article CAS PubMed Google Scholar
Van Geel M, Jacquemyn H, Plue J, Saar L, Kasari L, Peeters G, Van Acker K, Honnay O, Ceulemans T (2018) Abiotic rather than biotic filtering shapes the arbuscular mycorrhizal fungal communities of European seminatural grasslands. New Phytol 220:1262–1272. https://doi.org/10.1111/nph.14947
Article CAS PubMed Google Scholar
Vannette RL, Leopold DR, Fukami T (2016) Forest area and connectivity influence root-associated fungal communities in a fragmented landscape. Ecology 97:2374–2383. https://doi.org/10.1002/ecy.1472
Article PubMed Google Scholar
Warner NJ, Allen MF, MacMahon JA (1987) Dispersal agents of vesicular-arbuscular mycorrhizal fungi in a disturbed arid ecosystem. Mycologia 79:721–730. https://doi.org/10.2307/3807824
Article Google Scholar
Whytock RC, Fuentes-Montemayor E, Watts K, Andrade PB De, Whytock RT, French P, Macgregor NA, Park KJ (2017) Bird-community responses to habitat creation in a long-term, large-scale natural experiment. Conserv Biol 32:345–354. https://doi.org/10.1111/cobi.12983
Article PubMed Google Scholar
Willis A, Rodrigues BF, Harris PJC (2013) The ecology of arbuscular mycorrhizal fungi. Crit Rev Plant Sci 32:1–20. https://doi.org/10.1080/07352689.2012.683375
Article Google Scholar

Download references

Acknowledgements

We thank Willem Coudron for help with sampling and lab work, Gerrit Peeters for help with lab work and Kasper Van Acker for help with the soil analyses. This research was funded by the KU Leuven Research Fund (project C12/15/007).

Author information

Affiliations

Department of Biology, Plant Conservation and Population Biology, KU Leuven, 3001, Louvain, Belgium
Margaux Boeraeve, Olivier Honnay & Hans Jacquemyn

Authors

Margaux Boeraeve
View author publications
You can also search for this author in PubMed Google Scholar
Olivier Honnay
View author publications
You can also search for this author in PubMed Google Scholar
Hans Jacquemyn
View author publications
You can also search for this author in PubMed Google Scholar

Contributions

MB, OH and HJ designed the study. MB carried out field and lab work and did the analyses with support from OH and HJ. MB wrote the manuscript with support from OH and HJ.

Corresponding author

Correspondence to Margaux Boeraeve.

Additional information

Communicated by Joel Sachs.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 301 kb)

Supplementary material 2 (XLSX 55 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Boeraeve, M., Honnay, O. & Jacquemyn, H. Local abiotic conditions are more important than landscape context for structuring arbuscular mycorrhizal fungal communities in the roots of a forest herb. Oecologia 190, 149–157 (2019). https://doi.org/10.1007/s00442-019-04406-z

Download citation

Received: 15 April 2019
Accepted: 22 April 2019
Published: 11 May 2019
Issue Date: 01 May 2019
DOI: https://doi.org/10.1007/s00442-019-04406-z

Keywords

Arbuscular mycorrhizal fungi
Colonization
Habitat fragmentation
Land use change
Next generation sequencing