Abstract
More knowledge of community composition of arbuscular mycorrhizal (AM) fungi in ecosystems in relation to habitat type and land use intensity is needed. We studied AMF in 106 soil samples from pristine natural forests and a gradient of disturbance including semi-natural and intensively managed pastures of Terceira, Azores. Altogether, 42 spore morphotypes were detected from eight AMF families, revealing different fungal community structures among the three land use types. Spore density was highest in native forests and lowest in intensively managed pastures, but fungal richness was highest in semi-natural pastures and lowest in native forests. No significant difference occurred between intensively managed pastures and native forests. Members of Acaulosporaceae and Glomeraceae were dominant in native forests, while fungi from Gigasporaceae and Claroideoglomeraceae were most abundant in semi-natural and intensively managed pastures respectively, indicating family-based ecological preferences. Rarefaction analysis revealed that pastures supported more diverse AMF communities than native forests, because in high elevation pristine forests, a few rare species dominate. It is therefore likely that more species would be found with increasing survey effort. Further research is needed to clarify the influence of land use type on AMF diversity and distribution in remote islands, and the role of native AMF on soil ecosystem processes and the spread of exotic plants.
Similar content being viewed by others
References
Alcover JA, Pieper H, Pereira F et al (2015) Five new extinct species of rails (Aves: Gruiformes: Rallidae) from the Macaronesian Islands (North Atlantic Ocean). Zootaxa 4057:151–190. https://doi.org/10.11646/zootaxa.4057.2.1
Alguacil MM, Lumini E, Roldan A et al (2008) The impact of tillage practices on arbuscular mycorrhizal fungal diversity in subtropical crops. Ecol Appl 18:527–536. https://doi.org/10.1890/07-0521.1
Alguacil MM, Torrecillas E, García-Orenes F, Roldán A (2014) Changes in the composition and diversity of AMF communities mediated by management practices in a Mediterranean soil are related with increases in soil biological activity. Soil Biol Biochem 76:34–44. https://doi.org/10.1016/j.soilbio.2014.05.002
Álvarez-Sánchez J, Johnson NC, Antoninka A et al (2012) Large-scale diversity patterns in spore communities of arbuscular mycorrhizal fungi. In: Pagano M (ed) Mycorrhiza: occurrence in natural and restored environments. Nova Science Publishers, New York, pp 29–47
Ávila SP, Melo C, Berning B et al (2016) Persististrombus coronatus (Mollusca: Strombidae) in the lower Pliocene of Santa Maria Island (Azores, NE Atlantic): paleoecology, paleoclimatology and paleobiogeographic implications. Palaeogeogr Palaeocl 441:912–923. https://doi.org/10.1016/j.palaeo.2015.10.043
Avio L, Castaldini M, Fabiani A et al (2013) Impact of nitrogen fertilization and soil tillage on arbuscular mycorrhizal fungal communities in a Mediterranean agroecosystem. Soil Biol Biochem 67:285–294. https://doi.org/10.1016/j.soilbio.2013.09.005
Bainard LD, Bainard JD, Hamel C et al (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
Barea JM, Palenzuela J, Cornejo P et al (2011) Ecological and functional roles of mycorrhizas in semi-arid ecosystems of Southeast Spain. J Arid Environ 75:1292–1301. https://doi.org/10.1016/j.jaridenv.2011.06.001
Barea JM, Pozo MJ, Azcón R, Azcón-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778. https://doi.org/10.1093/jxb/eri197
Belay Z, Vestberg MV, Assefa F (2015) Diversity and abundance of arbuscular mycorrhizal fungi across different land use types in a humid low land area of Ethiopia. Trop Subtrop Agroecosystems 18:47–69
Birhane E, Fatumah N, Gidey K et al (2018) Vegetation cover density and disturbance affected arbuscular mycorrhiza fungi spore density and root colonization in a dry Afromontane forest, northern Ethiopia. J For Res 29:675–686. https://doi.org/10.1007/s11676-017-0493-5
Borges PAV (1997) Pasture arthropod community structure in Azorean islands of different geological age. Ph.D. Dissertation, Imperial College, University of London, London
Borriello R, Lumini E, Girlanda M et al (2012) Effects of different management practices on arbuscular mycorrhizal fungal diversity in maize fields by a molecular approach. Biol Fertil Soils 48:911–922. https://doi.org/10.1007/s00374-012-0683-4
Brito I, Goss MJ, de Carvalho M et al (2012) Impact of tillage system on arbuscular mycorrhiza fungal communities in the soil under Mediterranean conditions. Soil Tillage Res 121:63–67. https://doi.org/10.1016/j.still.2012.01.012
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
Brundrett MC, Abbott LK, Jasper DA (1999) Glomalean mycorrhizal fungi from tropical Australia. I. Comparison of the effectiveness and specificity of different isolation procedures. Mycorrhiza 8:305–314. https://doi.org/10.1007/s005720050251
Cai X-B, Peng Y-L, Yang M-N, et al (2014) Grassland degradation decrease the diversity of arbuscular mycorrhizal fungi species in Tibet Plateau. Not Bot Horti Agrobot Cluj-Napoca 42. doi: https://doi.org/10.15835/nbha.42.2.9458
Cardoso P, Lobo JM, Aranda SC et al (2009) A spatial scale assessment of habitat effects on arthropod communities of an oceanic island. Acta Oecol 35:90–597. https://doi.org/10.1016/j.actao.2009.05.005
Castillo CG, Rubio R, Rouanet JL, Borie F (2006) Early effects of tillage and crop rotation on arbuscular mycorrhizal fungal propagules in an Ultisol. Biol Fertil Soils 43:83–92. https://doi.org/10.1007/s00374-005-0067-0
Chen K, Weixin L, Guo S et al (2012) Diversity of arbuscular mycorrhizal fungi in continuous cropping soils used for pepper production. Afr J Microbiol Res 6:2469–2974. https://doi.org/10.5897/AJMR11.1532
Chen M, Arato M, Borghi L, et al (2018) Beneficial services of arbuscular mycorrhizal fungi—from ecology to application. Front Plant Sci 9:1270 https://doi.org/10.3389/fpls.2018.01270
Chitarra W, Pagliarani C, Maserti B et al (2016) Insights on the impact of arbuscular mycorrhizal symbiosis on tomato tolerance to water stress. Plant Physiol 171:1009–1023. https://doi.org/10.1104/pp.16.00307
Ciccolini V, Ercoli L, Davison J et al (2016) Land-use intensity and host plant simultaneously shape the composition of arbuscular mycorrhizal fungal communities in a Mediterranean drained peatland. FEMS Microbiol Ecol:92. https://doi.org/10.1093/femsec/fiw186
Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, second edn. PRIMER-E, Plymouth, UK
Colwell RK (2013) EstimateS: statistical estimation of species richness and shared species from samples. Version 9. User’s Guide and application published at: http://purl.oclc.org/estimates
Dai M, Bainard LD, Hamel C et al (2013) Impact of land use on arbuscular mycorrhizal fungal communities in rural Canada. Appl Environ Microbiol 79:6719–6729. https://doi.org/10.1128/AEM.01333-13
Davison J, Moora M, Öpik M et al (2015) Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349:970–973. https://doi.org/10.1126/science.aab1161
De Deyn GB, Quirk H, Bardgett RD (2011) Plant species richness, identity and productivity differentially influence key groups of microbes in grassland soils of contrasting fertility. Biol Lett 7:75–78. https://doi.org/10.1098/rsbl.2010.0575
Dias E (1996) Ecologia e sintaxonomia das florestas naturais (Ph.D. Dissertation). University of the Azores, Angra do Heroísmo
Dobo B, Asefa F, Asfaw Z (2016) Diversity of arbuscular mycorrhizal fungi of different plant species grown in three land use types in Wensho and Shebidino districts of Sidama in southern Ethiopia. Adv Biosci Bioeng 4:25. https://doi.org/10.11648/j.abb.20160404.11
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
Elias RB, Gil A, Silva L et al (2016) Natural zonal vegetation of the Azores Islands: characterization and potential distribution. Phytocoenologia 46:107–123. https://doi.org/10.1127/phyto/2016/0132
Faggioli VS, Cabello MN, Grilli G et al (2019) Root colonizing and soil borne communities of arbuscular mycorrhizal fungi differ among soybean fields with contrasting historical land use. Agric Ecosyst Environ 269:174–182. https://doi.org/10.1016/j.agee.2018.10.002
Gaspar C, Borges PA, Gaston KJ (2008) Diversity and distribution of arthropods in native forests of the Azores archipelago. Arquip Life Mar Sci 25:01–30
Gerz M, Bueno CG, Zobel M et al (2016) Plant community mycorrhization in temperate forests and grasslands: relations with edaphic properties and plant diversity. J Veg Sci 27:89–99. https://doi.org/10.1111/jvs.12338
Göhre V, Paszkowski U (2006) Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223:1115–1122. https://doi.org/10.1007/s00425-006-0225-0
González-Chávez MC, Carrillo-González R, Wright SF, Nichols KA (2004) The role of glomalin, a protein produced by arbuscular mycorrhizal fungi, in sequestering potentially toxic elements. Environ Pollut 130:317–323. https://doi.org/10.1016/j.envpol.2004.01.004
Hartmann M, Frey B, Mayer J et al (2015) Distinct soil microbial diversity under long-term organic and conventional farming. ISME J 9:1177–1194. https://doi.org/10.1038/ismej.2014.210
Hijri I, Sýkorová Z, Oehl F et al (2006) Communities of arbuscular mycorrhizal fungi in arable soils are not necessarily low in diversity. Mol Ecol 15:2277–2289. https://doi.org/10.1111/j.1365-294X.2006.02921.x
Hortal J, Borges PAV, Gaspar C (2006) Evaluating the performance of species richness estimators: sensitivity to sample grain size. J Anim Ecol 75:274–287. https://doi.org/10.1111/j.1365-2656.2006.01048.x
Hu J, Lin X, Wang J et al (2009) Arbuscular mycorrhizal fungus enhances crop yield and P-uptake of maize (Zea mays L.): a field case study on a sandy loam soil as affected by long-term P-deficiency fertilization. Soil Biol Biochem 41:2460–2465. https://doi.org/10.1016/j.soilbio.2009.09.002
IBM Corp (2013) IBM SPSS Statistics for Windows, Version 22.0. IBM Corp, Armonk, NY
Jamshidi S, Behm JE, Eveillard D et al (2015) Using hybrid automata modelling to study phenotypic plasticity and allocation strategies in the plant mycorrhizal mutualism. Ecol Model 311:11–19. https://doi.org/10.1016/j.ecolmodel.2015.04.021
Jansa J, Mozafar A, Anken T et al (2002) Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza 12:225–234. https://doi.org/10.1007/s00572-002-0163-z
Jansa J, Mozafar A, Kuhn G et al (2003) Soil tillage affects the community structure of mycorrhizal fungi in maize roots. Ecol Appl 13:1164–1176
Jansa J, Wiemken A, Frossard E (2006) The effects of agricultural practices on arbuscular mycorrhizal fungi. Geol Soc Lond Spec Publ 266:89–115. https://doi.org/10.1144/GSL.SP.2006.266.01.08
Jeffries P, Gianinazzi S, Perotto S et al (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soils 37:1–16
Johnson NC, Tilman D, Wedin D (1992) Plant and soil controls on mycorrhizal fungal communities. Ecology 73:2034–2042. https://doi.org/10.2307/1941453
Kawahara A, Ezawa T (2013) Characterization of arbuscular mycorrhizal fungal communities with respect to zonal vegetation in a coastal dune ecosystem. Oecologia 173:533–543. https://doi.org/10.1007/s00442-013-2622-y
Kim Y-C, Gao C, Zheng Y et al (2015) Arbuscular mycorrhizal fungal community response to warming and nitrogen addition in a semiarid steppe ecosystem. Mycorrhiza 25:267–276. https://doi.org/10.1007/s00572-014-0608-1
Kivlin SN, Hawkes CV, Treseder KK (2011) Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biol Biochem 43:2294–2303. https://doi.org/10.1016/j.soilbio.2011.07.012
Köhl L, Oehl F, van der Heijden MGA (2014) Agricultural practices indirectly influence plant productivity and ecosystem services through effects on soil biota. Ecol Appl 24:1842–1853. https://doi.org/10.1890/13-1821.1
König S, Wubet T, Dormann CF et al (2010) TaqMan real-time PCR assays to assess arbuscular mycorrhizal responses to field manipulation of grassland biodiversity: effects of soil characteristics, plant species richness, and functional traits. Appl Environ Microbiol 76:3765–3775. https://doi.org/10.1128/AEM.02951-09
Lazarevic B, Losak T, Manschadi AM (2018) Arbuscular mycorrhizae modify winter wheat root morphology and alleviate phosphorus deficit stress. Plant Soil Environ 64(2018):47–52. https://doi.org/10.17221/678/2017-PSE
Lekberg Y, Waller LP (2016) What drives differences in arbuscular mycorrhizal fungal communities among plant species? Fungal Ecol 24:135–138. https://doi.org/10.1016/j.funeco.2016.05.012
Li L-F, Zhang Y, Zhao Z-W (2007) Arbuscular mycorrhizal colonization and spore density across different land-use types in a hot and arid ecosystem, Southwest China. J Plant Nutr Soil Sci 170:419–425. https://doi.org/10.1002/jpln.200625034
Li X, Gai J, Cai X, et al (2013) Molecular diversity of arbuscular mycorrhizal fungi associated with two co-occurring perennial plant species on a Tibetan altitudinal gradient. Mycorrhiza 24:. doi: https://doi.org/10.1007/s00572-013-0518-7
Lin X, Feng Y, Zhang H et al (2012) Long-term balanced fertilization decreases arbuscular mycorrhizal fungal diversity in an arable soil in North China revealed by 454 pyrosequencing. Environ Sci Technol 46:5764–5771. https://doi.org/10.1021/es3001695
Lumini E, Orgiazzi A, Borriello R et al (2010) Disclosing arbuscular mycorrhizal fungal biodiversity in soil through a land-use gradient using a pyrosequencing approach. Environ Microbiol. https://doi.org/10.1111/j.1462-2920.2009.02099.x
Mafaziya F, Madawala S (2015) Abundance, richness and root colonization of arbuscular mycorrhizal fungi in natural and semi-natural land use types at upper Hantana. Ceylon J Sci Biol Sci 44:25. https://doi.org/10.4038/cjsbs.v44i1.7338
Magurran AE (2004) Measuring biological diversity. Blackwell Science, Oxford
Martins AM (1993) The Azores-westernmost Europe: where evolution can be caught red-handed. Mus Mun Funchal 2:181–198
Mathimaran N, Ruh R, Jama B et al (2007) Impact of agricultural management on arbuscular mycorrhizal fungal communities in Kenyan ferralsol. Agric Ecosyst Environ 119:22–32. https://doi.org/10.1016/j.agee.2006.06.004
Melo CD, Luna S, Krüger C et al (2017) Arbuscular mycorrhizal fungal community composition associated with Juniperus brevifolia in native Azorean forest. Acta Oecol 79:48–61. https://doi.org/10.1016/j.actao.2016.12.006
Melo CD, Walker C, Krüger C et al (2019) Environmental factors driving arbuscular mycorrhizal fungal communities associated with endemic woody plant Picconia azorica on native forest of Azores. Ann Microbiol 69:1309–1327. https://doi.org/10.1007/s13213-019-01535-x
Melo CD, Walker C, Rodríguez-Echeverría S et al (2014) Species composition of arbuscular mycorrhizal fungi differ in semi-natural and intensively managed pastures in an isolated oceanic island (Terceira, Azores). Symbiosis 64:73–85. https://doi.org/10.1007/s13199-014-0303-1
Minggui G, Tang M, Zhang Q et al (2012) Effects of climatic and edaphic factors on arbuscular mycorrhizal fungi in the rhizosphere of Hippophae rhamnoides in the Loess Plateau, China. Acta Ecol Sin 32:62–67. https://doi.org/10.1016/j.chnaes.2011.12.005
Minitab I (2000) Minitab: release 13 for Windows. Minitab Inc., State College, PA
Moora M, Davison J, Öpik M et al (2014) Anthropogenic land use shapes the composition and phylogenetic structure of soil arbuscular mycorrhizal fungal communities. FEMS Microbiol Ecol 90:609–621. https://doi.org/10.1111/1574-6941.12420
Ndoye F, Kane A, Mangaptché N, et al (2012) Changes in land use system and environmental factors affect arbuscular mycorrhizal fungal density and diversity, and enzyme activities in rhizospheric soils of Acacia senegal (L.) Willd. In: Int. Sch. Res. Not. https://www.hindawi.com/journals/isrn/2012/563191/.
Newbold T, Hudson LN, Hill SL et al (2015) Global effects of land use on local terrestrial biodiversity. Nature 520:45–50. https://doi.org/10.1038/nature14324
Oehl F, Laczko E, Bogenrieder A et al (2010) Soil type and land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biol Biochem 42:724–738. https://doi.org/10.1016/j.soilbio.2010.01.006
Oehl F, Sieverding E, Ineichen K et al (2005) Community structure of arbuscular mycorrhizal fungi at different soil depths in extensively and intensively managed agroecosystems. New Phytol 165:273–283. https://doi.org/10.1111/j.1469-8137.2004.01235.x
Olden JD (2006) Biotic homogenization: a new research agenda for conservation biogeography. J Biogeogr 33:2027–2039. https://doi.org/10.1111/j.1365-2699.2006.01572.x
Öpik M, Moora M, Liira J, Zobel M (2006) Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe: arbuscular mycorrhizal fungal communities around the globe. J Ecol 94:778–790. https://doi.org/10.1111/j.1365-2745.2006.01136.x
Öpik M, Vanatoa A, Vanatoa E et al (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
Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398. https://doi.org/10.1016/j.pbi.2007.05.004
QGIS Development Team (2016) QGIS geographic information system. Open Source Geospatial Foundation Project. Retrieved from http://qgis.osgeo.org
Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53. https://doi.org/10.1111/j.1469-8137.2006.01750.x
Rodríguez-Echeverría S, Teixeira H, Correia M et al (2017) Arbuscular mycorrhizal fungi communities from tropical Africa reveal strong ecological structure. New Phytol 213:380–390. https://doi.org/10.1111/nph.14122
Schmidt MH, Thies C, Nentwig W, Tscharntke T (2008) Contrasting responses of arable spiders to the landscape matrix at different spatial scales. J Biogeogr 35:157–166. https://doi.org/10.1111/j.1365-2699.2007.01774.x
Schneider S, Hartmann M, Enkerli J, Widmer F (2010) Fungal community structure in soils of conventional and organic farming systems. Fungal Ecol 3:215–224. https://doi.org/10.1016/j.funeco.2009.10.006
Schnoor TK, Lekberg Y, Rosendahl S, Olsson PA (2011) Mechanical soil disturbance as a determinant of arbuscular mycorrhizal fungal communities in semi-natural grassland. Mycorrhiza 21:211–220. https://doi.org/10.1007/s00572-010-0325-3
Seaby RMH, Henderson PA, Prendergast JR (2004) Community Analysis Package. Version 4.01. Pisces Conservation Ltd., http://www.pisces-conservation.com
Senés-Guerrero C, Schüßler A (2016) A conserved arbuscular mycorrhizal fungal core-species community colonizes potato roots in the Andes. Fungal Divers 77:317–333. https://doi.org/10.1007/s13225-015-0328-7
Shi Z, Wang F, Zhang K, Chen Y (2014) Diversity and distribution of arbuscular mycorrhizal fungi along altitudinal gradients in Mount Taibai of the Qinling Mountains. Can J Microbiol 60:811–818. https://doi.org/10.1139/cjm-2014-0416
Smith SE, Facelli E, Pope S, Andrew Smith F (2010) Plant performance in stressful environments: interpreting new and established knowledge of the roles of arbuscular mycorrhizas. Plant Soil 326:3–20. https://doi.org/10.1007/s11104-009-9981-5
Solís-Rodríguez URJ, Ramos-Zapata JA, Hernández-Cuevas L et al (2020) Arbuscular mycorrhizal fungi diversity and distribution in tropical low flooding forest in Mexico. Mycol Prog 19:195–204. https://doi.org/10.1007/s11557-019-01550-x
Steffan-Dewenter I, Nzenberg UM, Rger CB et al (2002) Scale-dependent effects of landscape context on three pollinator guilds. Ecology 83:1421–1432
Sun X, Su Y, Zhang Y et al (2013) Diversity of arbuscular mycorrhizal fungal spore communities and its relations to plants under increased temperature and precipitation in a natural grassland. Chin Sci Bull 58:4109–4119. https://doi.org/10.1007/s11434-013-5961-5
Terzopoulou S, Rigal F, Whittaker RJ et al (2015) Drivers of extinction: the case of Azorean beetles. Biol Lett 11:1–4. https://doi.org/10.1098/rsbl.2015.0273
Triantis KA, Borges PAV, Ladle RJ et al (2010) Extinction debt on oceanic islands. Ecography 33:–285, 294. https://doi.org/10.1111/j.1600-0587.2010.06203.x
Turrini A, Giovannetti M (2012) Arbuscular mycorrhizal fungi in national parks, nature reserves and protected areas worldwide: a strategic perspective for their in situ conservation. Mycorrhiza 22:81–97. https://doi.org/10.1007/s00572-011-0419-6
van der Gast CJ, Gosling P, Tiwari B, Bending GD (2011) Spatial scaling of arbuscular mycorrhizal fungal diversity is affected by farming practice. Environ Microbiol 13:241–249. https://doi.org/10.1111/j.1462-2920.2010.02326.x
van der Heijden MGA, Martin FM, Selosse M-A, 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
Velázquez MS, Cabello MN, Barrera M (2013) Composition and structure of arbuscular-mycorrhizal communities in El Palmar National Park, Argentina. Mycologia 105:509–520. https://doi.org/10.3852/11-353
Verbruggen E, Toby Kiers E (2010) Evolutionary ecology of mycorrhizal functional diversity in agricultural systems: AMF in agriculture. Evol Appl 3:547–560. https://doi.org/10.1111/j.1752-4571.2010.00145.x
Violi HA, Barrientos-Priego AF, Wright SF et al (2008) Disturbance changes arbuscular mycorrhizal fungal phenology and soil glomalin concentrations but not fungal spore composition in montane rainforests in Veracruz and Chiapas, Mexico. For Ecol Manag 254:276–290. https://doi.org/10.1016/j.foreco.2007.08.016
Vos CM, Tesfahun AN, Panis B et al (2012) Arbuscular mycorrhizal fungi induce systemic resistance in tomato against the sedentary nematode Meloidogyne incognita and the migratory nematode Pratylenchus penetrans. Appl Soil Ecol 61:1–6. https://doi.org/10.1016/j.apsoil.2012.04.007
Wang YY, Vestberg M, Walker C, Hurme T, Zhang X, Lindström K (2008) Diversity and infectivity of arbuscular mycorrhizal fungi in agricultural soils of the Sichuan Province of mainland China. Mycorrhiza 18:59–68. doi.org/10.1007/s00572-008-0161-x
Xiang D, Verbruggen E, Hu Y et al (2014) Land use influences arbuscular mycorrhizal fungal communities in the farming-pastoral ecotone of northern China. New Phytol 204:968–978. https://doi.org/10.1111/nph.12961
Xu X, Chen C, Zhang Z et al (2017) The influence of environmental factors on communities of arbuscular mycorrhizal fungi associated with Chenopodium ambrosioides revealed by MiSeq sequencing investigation. Sci Rep 7:45134. https://doi.org/10.1038/srep45134
Yang H, Zang Y, Yuan Y et al (2012) Selectivity by host plants affects the distribution of arbuscular mycorrhizal fungi: evidence from ITS rDNA sequence metadata. BMC Evol Biol 12:1
Zangaro W, de Assis RL, Rostirola LV et al (2008) Changes in arbuscular mycorrhizal associations and fine root traits in sites under different plant successional phases in southern Brazil. Mycorrhiza 19:37–45. https://doi.org/10.1007/s00572-008-0202-5
Zar J (1999) Biostatistical analysis 4th edition. Prentice-Hall International, Upper Saddle River, NJ
Zhang S, Li Q, Lü Y et al (2013) Contributions of soil biota to C sequestration varied with aggregate fractions under different tillage systems. Soil Biol Biochem 62:147–156. https://doi.org/10.1016/j.soilbio.2013.03.023
Zheng Y, Chen L, Luo C-Y et al (2016) Plant identity exerts stronger effect than fertilization on soil arbuscular mycorrhizal fungi in a sown pasture. Microb Ecol 72:647–658. https://doi.org/10.1007/s00248-016-0817-6
Zheng Y, Kim Y-C, Tian X-F et al (2014) Differential responses of arbuscular mycorrhizal fungi to nitrogen addition in a near pristine Tibetan alpine meadow. FEMS Microbiol Ecol 89:594–605. https://doi.org/10.1111/1574-6941.12361
Acknowledgements
The authors would like to thank to the Regional Directorate for Forest Resources for field sites support.
Availability of data and materials
All data generated or analysed during this study are included in this published article.
Adherence to national and international regulations
Not applicable.
Funding
This research was funded by Fundo Regional para a Ciência e Tecnologia–Governo dos Açores (M3.1.a/F/059/2016; M3.1.a/F/012/2016) and by the Development Grant (IF/00462/2013) from the Fundação para a Ciência e a Tecnologia (FCT) Portugal with national funds and co-funded by FEDER and COMPETE 2020 program. The Royal Botanic Garden Edinburgh (RBGE) is supported by the Scottish Government’s Rural and Environmental Science and Analytical Services Division.
Author information
Authors and Affiliations
Contributions
Conceptualisation, CDM; investigation, CDM; AMF identification, CDM and CW; formal analysis, CDM, RP and PAVB; writing—original draft preparation, CDM and RP; writing—review and editing, CDM, RP, CW, SR-E, HF and PAVB; and PAVB and HF supervised the development of this work. All authors interpreted the results and contributed to the final manuscript and CDM led the writing of the manuscript. All authors gave final approval for publication.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Section Editor: Marco Thines
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Melo, C.D., Pimentel, R., Walker, C. et al. Diversity and distribution of arbuscular mycorrhizal fungi along a land use gradient in Terceira Island (Azores). Mycol Progress 19, 643–656 (2020). https://doi.org/10.1007/s11557-020-01582-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11557-020-01582-8