Abstract
Our aim was to test if ecological stages may influence the arbuscular mycorrhizal fungi (AMF), nematodes, and the soil chemical properties in agroforestry systems (AF), unassisted forest restoration (UFR), and natural ecosystem (Ne) located in the Brazilian Tropical and Subtropical regions. We collected soil samples to determine AMF, nematodes, soil pH, P, and soil organic carbon (SOC). AMF and nematode richness in the AF and Ne were similar in the tropical region. The redundancy analysis (RDA) indicated that the abundance of AMF and soil nematodes was mainly affected by soil pH, P, and SOC. Differences were associated with (1) ecological stages, as we found differences in AMF and nematode abundance as affected by habitat simplification, and (2) changes in soil pH, SOC, and P. Our work increases the understanding of the AMF and soil nematode community in the rhizosphere of AF and Ne in tropical and subtropical regions.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data sharing is applicable with a formal and justified request for the corresponding author.
References
Akinde BP, Olakayode AO, Oyedele DJ, Tijani OF (2020) Selected physical and chemical properties of soil under different agricultural land-use types in Ile-Ife, Nigeria. Heliyon. https://doi.org/10.1016/j.heliyon.2020.e05090
Anderson JM, Ingram JSI (1993) Tropical soil biology and fertility: a handbook of methods. CAB International, Wallingford, p 12
Black CA, Evans DD, Ensminger LE, White JL, Clark FE, Dinauer RC (1965) Methods of soil analysis. In: Black CA, Evans DD, Ensminger LE, White JL, Clark FE, Dinauer RC (eds) Chemical and microbiological properties, 2nd edn. Soil Science Society of America International Publisher, Madison, p 160
Buchan D, Gebremikael MT, Ameloot N, Sleutel S, Neve S (2013) The effect of free-living nematodes on nitrogen mineralisation in undisturbed and disturbed soil cores. Soil Biol Biochem 60:142–155. https://doi.org/10.1016/j.soilbio.2013.01.022
Caifa AN, Martins FR (2007) Taxonomic identification, sampling methods, and minimum size of the tree sampled: implications and perspectives for studies in the Brazilian Atlantic Rainforest. Funct Ecosyst Commun 1(2):95–104
Chen X, Chen HYH, Chen C, Ma Z, Searle EB, Yu Z, Huang Z (2020) Effects of plant diversity on soil carbon in diverse ecosystems: a global meta-analysis. Biol Rev 95(1):167–183. https://doi.org/10.1111/brv.12554
Chernov TI, Zhelenova AD, Tkhakakhova AK, Ksenofontova NA, Zverev AO, Tiunov AV (2021) Soil microbiome, organic matter content and microbial abundance in forest and forest-derived land cover in Cat Tien National Park (Vietnam). Appl Soil Ecol 165:103957. https://doi.org/10.1016/j.apsoil.2021.103957
Costa IR, Araújo FS (2007) Organização comunitária de um encrave de cerrado sensu stricto no bioma Caatinga, chapada do Araripe, Barbalha Ceará. Acta Bot Bras. https://doi.org/10.1590/S0102-33062007000200004
Daubenmire RE (1968) Plant communities: a textbook of plant synecology. Harper and Row, New York
Dierks J, Blaser-Harta WJ, Gamper HA, Nyok IB, Barrios E, Six J (2021) Trees enhance abundance of arbuscular mycorrhizal fungi, soil structure, and nutrient retention in low-input maize cropping systems. Agric Ecosyst Environ 318:107487. https://doi.org/10.1016/j.agee.2021.107487
Forstall-Sosa KS, Souza TAF, Lucena EO, da Silva SAI, Ferreira JTA, Silva TN, Santos D, Niemeyer JC (2020) Soil macroarthropod community and soil biological quality index in a green manure farming system of the Brazilian semi-arid. Biologia 76(3):907–917. https://doi.org/10.2478/s11756-020-00602-y
Fu D, Wu X, Qiu Q, Duan C, Jones D (2020) Seasonal variations in soil microbial communities under different land restoration types in a subtropical mountains region, Southwest China. Appl Soil Ecol 153:103634. https://doi.org/10.1016/j.apsoil.2020.103634
Gao G, Liu Z, Wang Y, Wang S, Ju C, Gu J (2020) Tamm review: fine root biomass in the organic (O) horizon in forest ecosystems: Global patterns and controlling factors. For Ecol Manag 491:119208. https://doi.org/10.1016/j.foreco.2021.119208
Gerdemann JW, Nicolson TH (1963) Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Trans Br Mycol Soc 46(2):235–244. https://doi.org/10.1016/S0007-1536(63)80079-0
Gilarte P, Plett J, Pendall E, Carrillo Y, Nielsen UN (2020) Direct and indirect trophic interactions of soil nematodes impact chickpea and oat nutrition. Plant Soil 457:255–268. https://doi.org/10.1007/s11104-020-04735-6
Gittleman JL, Kot M (1990) Adaptation: statistics and a null model for estimating phylogenetic effects. Syst Zool 39(3):227–241. https://doi.org/10.2307/2992183
Hu P, Xiao J, Zhang W, Xiao L, Yang R, Xiao D, Zhao J, Wang K (2020) Response of soil microbial communities to natural and managed vegetation restoration in a subtropical karst region. CATENA 195:104849. https://doi.org/10.1016/j.catena.2020.104849
Inague GM, Zwiener VP, Marques MCM (2021) Climate change threatens the woody plant taxonomic and functional diversities of the Restinga vegetation in Brazil. Perspec Ecol Conserv 19:53–60. https://doi.org/10.1016/j.pecon.2020.12.006
IUSS Working Group WRB. 2015 International Soil Classification System for Naming Soils and Creating Legends for Soil Maps; World Reference Base for Soil Resources 2014; World Soil Resources Reports No. 106; FAO: Rome, Italy.
Jenkins W (1964) A rapid centrifugal-flotation technique for separating nematodes from soil. Plant Dis Rep 48:692
Kooch Y, Ehsani S, Akbarinia M (2020) Stratification of soil organic matter and biota dynamics in natural and anthropogenic ecosystems. Soil Tillage Res 200:204621. https://doi.org/10.1016/j.still.2020.104621
Kou X, Ma N, Zhang X, Xie H, Zhang X, Wu Z, Liang W, Li Q, Ferris H (2020) Frequency of stover mulching but not amount regulates the decomposition pathways of soil micro-food webs in a no-tillage system. Soil Biol Biochem. https://doi.org/10.1016/j.soilbio.2020.107789
Lance AC, Carrino-Kyker SR, Burke DJ, Burns JH (2020) Individual plant-soil feedback effects influence tree growth and rhizosphere fungal communities in a temperate forest restoration experiment. Front Ecol Evol. https://doi.org/10.3389/fevo.2019.00500
Laurindo LK, Souza TAF, Silva LJR, Kormann S, Pires KJC, Casal TB (2020) Nematoides. In: Laurindo LK, Souza TAF, Silva LJR, Kormann S, Pires KJC, Casal TB (eds) Indicadores da qualidade do solo em sistemas agroflorestais e ecossistemas associados, 1st edn. PPGEAN: USFC, Florianópolis
Laurindo LK, Souza TAF, Silva LJR, Casal TB, Pires KJC, Kormann Schmitt DE, Siminski A (2021) Arbuscular mycorrhizal fungal community assembly in agroforestry systems from the Southern Brazil. Biologia 76:1099–1107. https://doi.org/10.1007/s11756-021-00700-5
Le Provost G, Thiele J, Westphal C, Penone C, Allan E, Neyret M, van der Plas F, Ayasse M, Bardgett RD, Birkhofer K, Bich S, Bonkowski M, Buscot F, Feldhaar H, Gaulton R, Goldmann K, Gossener MM, Klaus VH, Kleinebecker T, Krauss J, Renner S, Scherreiks P, Sikorski J, Baulechner D, Blüthgen N, Bolliger R, Börsching C, Busch V, Chisté M, Fiore-Donno AM, Fischer M, Arndt H, Hoelzel N, John K, Jung K, Lange M, Marzini C, Overmann J, Paŝalić E, Perović DJ, Prati D, Schäfer D, Schrumpf M, Sonnermann I, Steffan-Dewenter I, Tschapka M, Türke M, Vogt J, Wehner K, Weiner C, Weisser W, Wells K, Werner M, Wolters V, Wubet T, Wurts S, Zaitsey AS, Manning P (2021) Contrasting responses of above- and belowground diversity to multiple components of land-use intensity. Nat Commun. https://doi.org/10.1038/s41467-021-23931-1
Liu Y, Zhu G, Hai X, Li J, Shangguan Z, Peng C, Deng L (2020) Long-term forest succession improves plant diversity and soil quality but not significantly increase soil microbial diversity: evidence from the Loess Plateau. Ecol Eng. https://doi.org/10.1016/j.ecoleng.2019.105631
Lucena EO, Souza TAF, Araújo JS, Andrade LA, Santos D, Podestá GS (2018) Occurrence and distribution of Gigaspora under Cryptostegia madagascariensis Bojer Ex Decne in Brazilian tropical seasonal dry forest. Agrotec 39(3):221–227. https://doi.org/10.25066/agrotec.v39i3.40055
Lucena EO, Souza T, Silva SIA, Kormann S, Silva LJR, Laurindo LK, Forstall-Sosa KS, Andrade LA (2021) Soil biota community composition as affected by Cryptostegia madagascariensis invasion in a tropical Cambisol from North-eastern Brazil. Trop Ecol. https://doi.org/10.1007/s42965-021-00177-y
Melo LN, Souza TAF, Santos D (2019) Transpiratory rate, biomass production, and leaf macronutrient content of different plant species cultivated on a Regosol in the Brazilian semiarid. Russ Agric Sci 45(2):147–153. https://doi.org/10.3103/S1068367419020150
Melo CD, Pimentel R, Walker C, Rodríguez-Echeverría S, Freitas H, Borges PAV (2020) Diversity and distribution of arbuscular mycorrhizal fungi along a land use gradient in Terceira Island (Azores). Mycol Prog 19(7):643–656. https://doi.org/10.1007/s11557-020-01582-8
Melo VF, Barros LS, Silva MCS, Veloso TGR, Senwo ZN, Matos KS, Nunes TKO (2021) Soil bacterial diversities and response to deforestation, land use and burning in North Amazon, Brazil. Appl Soil Ecol 2021:158. https://doi.org/10.1016/j.apsoil.2020.103775
Muchane MN, Sileshi GW, Gripenberge S, Jonsson M, Pumariño L, Barrios E (2020) Agroforestry boosts soil health in the humid and sub-humid tropics: a meta-analysis. Agric Ecosyst Environ. https://doi.org/10.1016/j.agee.2020.106899
Nascimento GS, Souza TAF, Silva LJR, Santos D (2021) Soil physico-chemical properties, biomass production, and root density in a green manure farming system from tropical ecosystem, North-Eastern Brazil. J Soils Sediments 21(6):2203–2211. https://doi.org/10.1007/s11368-021-02924-z
Neilson R, Caul S, Fraser FC, King D, Mitchell SM, Roberts DM, Giles ME (2020) Microbial community size is a potential predictor of nematode functional group in limed grasslands. Appl Soil Ecol. https://doi.org/10.1016/j.apsoil.2020.103702
Nisa RU, Tantray AY, Kouser N, Allie KA, Wani SM, Alamri SA, Alymeni MN, Wijava L, Shah AA (2021) Influence of ecological and edaphic factors on biodiversity of soil nematodes. Saud J Biol Sci 28:3049–3059. https://doi.org/10.1016/j.sjbs.2021.02.04
Okalebo JR, Gathua KW, Woomer PL (1993) Laboratory methods of plant and soil analysis: a working manual, 2nd edn. SACRED Africa, Nairobi, p 127
Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA Circ 939:1–19
Ossowicki A, Raaijmakers JM, Garbeva P (2021) Disentangling soil microbiome functions by perturbation. Environ Microbiol Rep. https://doi.org/10.1111/1758-2229.12989
Peralta G, Dickie IA, Yeates GW, Peltzer DA (2020) Community- and trophic-level responses of soil nematodes to removal of a non-native tree at different stages of invasion. PLoS ONE. https://doi.org/10.1371/journal.pone.0227130
Pinheiro ES, Durigan G (2012) Diferenças florísticas e estruturais entre fitofisionomias do cerrado em Assis, Sp, Brasil. Rev Árvore. https://doi.org/10.1590/S0100-67622012000100019
Pyles MV, Magnago LFS, Borges ER, van den Berg E, Carvalho FA (2020) Land use history drives differences in functional composition and losses in functional diversity and stability of Neotropical urban forests. Urban Urban Green. https://doi.org/10.1016/j.ufug.2020.126608
R Core Team. A language and Environment for statistical computing. R Core Tem 2018. http://www.rproject.org/, Accessed 17 October 2021
Raiesi F, Salek-Gilani S (2020) Development of a soil quality index for characterizing effects of land-use changes on degradation and ecological restoration of rangeland soils in a semi- arid ecosystem. Land Deg Dev 31(12):1533–1544. https://doi.org/10.1002/ldr.3553
Reichert JM, Gubiani PI, Santos DR, Reinert DJ, Aita C, Giacomini SJ (2021) Soil properties characterization for land-use planning and soil management in watersheds under family farming. Int Soil Water Conserv Res 10:119–128. https://doi.org/10.1016/j.iswcr.2021.05.003
Schenck NC, Pérez Y (1990) Manual for the identification of VA Mycorrhizal Fungi. Synergistic, Gainesville
Siebert J, Ciobanu M, Schädler M, Eisenhauer N (2020) Climate change and land use induce functional shifts in soil nematode communities. Oecologia 192:281–294. https://doi.org/10.1007/s00442-019-04560-4
Silva SIA, Souza TAF, Lucena EO, Silva LJR, Laurindo LK, Nascimento GS, Santos D (2021) High phosphorus availability promotes the diversity of arbuscular mycorrhizal spores’ Community in different tropical ecosystem. Biologia 76:3211–3220. https://doi.org/10.1007/s11756-021-00874-y
Singh AK, Jiang X, Yang B, Wu J, Rai A, Chen C, Ahirwal J, Wang P, Liu W, Singh N (2021) Biological indicators affected by land use change, soil resource availability and seasonality in dry tropics. Ecol Indic 115:106396. https://doi.org/10.1016/j.ecolind.2020.106369
Souza T (2015) Handbook of Arbuscular Mycorrhizal Fungi, 1st edn. Springer International Publishing, Cham. https://doi.org/10.1007/978-3-319-24850-9
Souza TAF, Freitas H (2018) Arbuscular mycorrhizal fungal community assembly in the Brazilian tropical seasonal dry forest. Ecol Process. https://doi.org/10.1186/s13717-017-0072-x
Souza TAF, Dobner Junior M, Schmitt DE, Silva LJR, Schneider K (2022) Soil biotic and abiotic characteristics as driven factors for site quality of Araucaria angustifolia plantations. Biologia. https://doi.org/10.1007/s11756-021-00988-3
Tedersoo L, Sanchez-Ramírez S, Kõljalg U, Bahram M, Dõring M, Schigel D, May T, Ryberg M, Abarenkov K (2018) High-level classification of the Fungi and a tool for evolutionary ecological analyses. Fungal Divers 90:135–159. https://doi.org/10.1007/s13225-018-0401-0
Teixeira HM, Bianchi FJJA, Cardoso IM, Tittonell P, Peña-Claros M (2021) Impact of agroecological management on plant diversity and soil-based ecosystem services in pasture and coffee systems in the Atlantic Forest of Brazil. Agric Ecosyst Environ. https://doi.org/10.1016/j.agee.2020.107171
Terefe D, Belay Z, Assefa F, Kibret K, Dechassa N (2021) Abundance and diversity of arbuscular mycorrhizal fungi (AMF) in soils under different rangeland use types in the middle Awash Basin, Ethiopia. East Afr J Sci 15(1):25–40
Timper P, Strickland TC, Jagdale GB (2021) Biological suppression of the root-knot nematode Meloidogyne incognita following winter cover crops in conservation tillage cotton. Biol Control. https://doi.org/10.1016/j.biocontrol.2020.104525
Wahdan SFM, Heintz-Buschart A, Sansupa C, Tanunchai B, Wu Y, Schädler M, Noll M, Purahong W, Buscot F (2021) Targeting the active rhizosphere microbiome of Trifolium pratense in grassland evidences a stronger-than-expected belowground biodiversity ecosystem functioning link. Front Microbiol. https://doi.org/10.3389/fmicb.2021.629169
Wang J, Wang J, He J, Zhu Y, Qiao N, Ge Y (2021) Arbuscular mycorrhizal fungi and plant diversity drive restoration of nitrogen-cycling microbial communities. Mol Ecol 30(16):4133–4146. https://doi.org/10.1111/mec.16030
Wilschut RA, Geisen S (2020) Nematodes as drivers of plant performance in natural systems. Trends Plant Sci 26(3):237–247. https://doi.org/10.1016/j.tplants.2020.10.006
Wu Y, Chen W, Entemake W, Wang J, Liu H, Zhao Z, Li Y, Qiao L, Yang B, Liu G, Xue S (2021) Long-term vegetation restoration promotes the stability of the soil micro-food web in the Loess Plateau in North-west China. CATENA. https://doi.org/10.1016/j.catena.2021.105293
Yamauchi DH, Garces HG, Teixeira MM, Rodrigues GFB, Ullmann LS, Garces AG, Hebeler-Barbosa F, Bagagli E (2021) Soil mycobiome is shaped by vegetation and microhabitats: a regional-scale study in Southeastern Brazil. J Fungi 7(8):587. https://doi.org/10.3390/jof7080587
Yang B, Banerjee S, Herzog C, Ramirez AC, Dahlin P, van der Heijden MGA (2021) Impact of land use type and organic farming on the abundance, diversity, community composition and functional properties of soil nematode communities in vegetable farming. Agric Ecosyst Environ. https://doi.org/10.1016/j.agee.2021.107488
Yao MK, Koné AW, Otinga NA, Kassin EK, Tano Y (2021) Carbon and nutrient cycling in tree plantations vs. natural forests: implication for an efficient cocoa agroforestry system in West Africa. Reg Environ Change. https://doi.org/10.1007/s10113-021-01776-0
Ye Y, Rui Y, Zeng Z, He X, Wang K, Zhao J (2020) Responses of soil nematode community to monoculture or mixed culture of a grass and a legume forage species in China. Pedosphere 30(6):791–800. https://doi.org/10.1016/S1002-0160(20)60039-X
Yeates GW, Bongers T, Goede RGM, Freckman DW, Georgieva SS (1993) Feeding habits in soil nematode families and genera—An outline for soil ecologists. J Nematol 25:315–331
Yinga OE, Kumar KS, Chowlani M, Tripathi SK, Khanduri VP, Singh SK (2020) Influence of land-use pattern on soil quality in a steeply sloped tropical mountainous region. India Arch Agron Soil Sci. https://doi.org/10.1080/03650340.2020.1858478
Zarafshar M, Bazot S, Matinizadeh M, Bordbar SK, Rousta MJ, Kooch Y, Enayati K, Abbasi A, Negahdarsaber M (2020) Do tree plantations or cultivated fields have the same ability to maintain soil quality as natural forests? Appl Soil Ecol. https://doi.org/10.1016/j.apsoil.2020.103536
Zhang K, Landry GM, Liao HL (2021a) How soil biota regulate C cycling and soil C pools in diversified crop rotations. Soil Biol Biochem. https://doi.org/10.1016/j.soilbio.2021.108219
Zhang J, Quan C, Ma L, Chu G, Liu Z, Tang X (2021b) Plant community and soil properties drive arbuscular mycorrhizal fungal diversity: a case study in tropical forests. Soil Ecol Lett 3(2):52–62. https://doi.org/10.1007/s42832-020-0049-z
Acknowledgements
We thank the GEBIOS (Soil Biology Research Group) for practical support. We thank the Postgraduate Program of Soil Science of the Federal University of Paraiba for facilitating the post-doc studies of the first author. Tancredo Souza is supported by a Research fellowship from FAPESQ-Brazil. Lucas Jónatan Rodrigues da Silva, and Lídia Klestadt Laurindo benefited from a scholarship provided by FAPESC and CNPq, respectively.
Funding
This work was partly funded by the FAPESQ-Brazil.
Author information
Authors and Affiliations
Contributions
Conceptualization, TAFS; methodology, TAFS, LJRS, LKL, GSN, and MCCC; software, TAFS, and MCCC; formal analysis, LJRS, and LKL; investigation, TAFS, LJRS, LKL, and GSN; resources, TAFS, and MCCC; data curation, TAFS; writing—original draft preparation, TAFS, LJRS, LKL, GSN, and MCCC; writing—review and editing, TAFS, LJRS, and MCCC; visualization, TAFS, LJRS, LKL, GSN, and MCCC; supervision, TAFS; project administration, TAFS; funding acquisition, TAFS. All authors have read and agreed to the published version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Communicated by Ran Wang.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
de Souza, T.A.F., da Silva, L.J.R., Laurindo, L.K. et al. Impact of ecological stages on the soil microbiota and soil abiotic factors in tropical and subtropical Brazilian regions. Arch Microbiol 205, 335 (2023). https://doi.org/10.1007/s00203-023-03677-8
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-023-03677-8