ABSTRACT
Canga ecosystems develop over superficial iron crusts with shallow and nutrient-poor soils. Under these conditions, arbuscular mycorrhizal fungi (AMF) play an important role in helping plants to overcome abiotic and biotic stresses. Canga can suffer periodic burning and yet it is unknown what the impacts of fire are to AMF communities. We aimed to compare AMF in Canga areas affected by burning (BC) with those with no previous history of burning (NC). We compared AMF species composition, spore numbers, species richness, and mycorrhizal inoculum potential. The total number of spores, AMF species richness and mycorrhizal colonization measured in the infectivity bioassay were not significantly different between areas. A total of 23 species in 10 genera were recovered, with most species belonging to Gigasporaceae and Acaulosporaceae. BC and NC shared 52 % of AMF species. Gigaspora albida, Gigaspora gigantea, and Dentiscutata heterogama sporulated exclusively in trap cultures. We concluded that AMF spore communities were not affected by burning in Canga soils as measured by spore abundance, species richness and infectivity. Our data contribute to the inventory of soil biodiversity associated with Canga, a high biodiverse and threatened Brazilian ecosystem.
Keywords:
Acaulosporaceae; Canga; Gigasporaceae; Glomeromycota; inoculum potential; mycorrhiza; spore numbers; taxonomic diversity; trap cultures
Introduction
Canga ecosystems are associated with superficial iron crust occurring in Minas Gerais and Pará states in Brazil. These ecosystems are dominated by grasses and sages mixed with shrubs growing on fragmented iron crust and perennial and annual herbs developing in rock crevices. Plant families that dominate in this ecosystem are Poaceae, Asteraceae, Fabaceae, Myrtaceae, and Melastomataceae (Skirycz et al. 2014Skirycz A, Castilho A, Chaparro C, Carvalho N, Tzotzos G, Siqueira JO. 2014. Canga biodiversity, a matter of mining. Frontiers in Plant Sciences 5: 1-9. ). This ecosystem thrives under severe environmental conditions such as high ultraviolet exposure and daily temperatures, strong winds, rapid water loss, and shallow acidic nutritionally-poor soils that can contain toxic levels of aluminum and heavy metals (Jacobi et al. 2007Jacobi CM, Carmo FF, Vincent RC, Stehmann JR. 2007. Plant communities on the ironstone outcrops - a diverse and endangered Brazilian ecosystem. Biodiversity and Conservation 16: 2185-2220.; Skirycz et al. 2014Skirycz A, Castilho A, Chaparro C, Carvalho N, Tzotzos G, Siqueira JO. 2014. Canga biodiversity, a matter of mining. Frontiers in Plant Sciences 5: 1-9. ). Distinct microhabitats can be formed in Canga, mainly due to its occurrence along mountain tops, which contributes to the high alpha and beta diversity of plant communities. For this reason, it is considered an ecosystem with high biodiversity (Skirycz et al. 2014Skirycz A, Castilho A, Chaparro C, Carvalho N, Tzotzos G, Siqueira JO. 2014. Canga biodiversity, a matter of mining. Frontiers in Plant Sciences 5: 1-9. ). Studies in Canga include the diversity of plant communities (Giulietti et al. 2019Giulietti AM, Giannini TC, Mota NFO, et al. 2019. Edaphic endemism in the Amazon: vascular plants of the canga of Carajás, Brazil. The Botanical Review 24: 357-383.; Andrino et al. 2020Andrino CO, Barbosa-Silva RG, Lovo J, Viana PL, Moro MF, Zappi DC. 2020. Iron islands in the Amazon: investigating plant beta diversity of canga outcrops. PhytoKeys 165: 1-25.), soil fauna (Oliveira et al. 2019Oliveira MPA, Bastos-Pereira R, Torres SHS, et al. 2019. Choosing sampling methods for Chilopoda, Diplopoda and Isopoda (Oniscidea): A case study for ferruginous landscapes in Brazilian Amazonia. Applied Soil Ecology 143: 181-191.), and plant growth-promoting bacteria (Felestrino et al. 2018Felestrino EB, Vieira IT, Caneschi WL, et al. 2018. Biotechnological potential of plant growth-promoting bacteria from the roots and rhizospheres of endemic plants in ironstone vegetation in southeastern Brazil. World Journal of Microbiology and Biotechnology 24: 156.; Silva et al. 2020Silva AO, Guimarães AA, Costa AM, et al. 2020. Plant growth-promoting rhizobacterial communities from an area under the influence of iron mining and from the adjacent phytophysiognomies which have high genetic diversity. Land Degradation and Development 31: 2237-2254.). Surveys towards conservation and management purposes were also developed in this ecosystem (Souza-Filho et al. 2019Souza-Filho PWM, Giannini TC, Jaffé R, et al. 2019. Mapping and quantification of ferruginous outcrops savannas in the Brazilian Amazon: A challenge for biodiversity conservation. PLOS ONE 14: e0211095. ; Barbosa et al. 2020Barbosa LC, Viana PL, Teodoro GS, Caldeira CF, Ramos SJ, Gastauer M. 2020. A wildfire in an Amazonian canga community maintained important ecosystem properties. International Journal of Wildland Fire 29: 943-949.). Plant communities in Canga resemble savanna vegetation due to the dominance of herbaceous plants, shrubs, and few trees (Skirycz et al. 2014Skirycz A, Castilho A, Chaparro C, Carvalho N, Tzotzos G, Siqueira JO. 2014. Canga biodiversity, a matter of mining. Frontiers in Plant Sciences 5: 1-9. ). However, information on communities of arbuscular mycorrhizal fungi (AMF) associated with the vegetation occurring in Canga is scarce.
Arbuscular mycorrhizal fungi are soil fungi commonly associated with plants in terrestrial and aquatic ecosystems (Smith & Read 2008Smith SE, Read DJ. 2008. Mycorrhizal Symbiosis. 3rd. edn. New York, Academic Press. ). These fungi help plants overcoming abiotic and biotic stress by improving nutrient uptake (especially phosphorus), improving soil aggregation, and decreasing nutrient leaching from the environment (Rillig & Mummey 2006Rillig MC, Mummey DL. 2006. Mycorrhizas and soil structure. New Phytologist 171: 41-53.; Gianinazzi et al. 2010Gianinazzi S, Gollotte A, Binet MN, Tuinen D, Redecker D, Wipf D. 2010. Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20: 519-530.; Verbruggen et al. 2012Verbruggen E, van der Heijden MGA, Rillig MC, Kiers T. 2012. Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success. New Phytologist 197: 1104-1109.). Studies of occurrence and distribution of AMF in Brazilian ecosystems associated with different floristic domains revealed a high diversity of these fungi associated with natural vegetation, agroecosystems, and disturbed sites (Stürmer & Siqueira 2008Stürmer SL, Siqueira JO. 2008. Diversidade de Fungos Micorrízicos Arbusculares em Ecossistemas Brasileiros. In: Moreira FMS, Siqueira JO, Brussaard L. (eds.) Biodiversidade do solo em ecossistemas brasileiros. Lavras, Editora UFLA. p. 537-584.; Maia et al. 2020Maia LC, Passos JH, Silva JÁ, Oehl F, Assis DMA. 2020. Species diversity of Glomeromycota in Brazilian biomes. Sydowia 72: 181-205.). Natural non-burned plots of Canga have been surveyed for AMF communities by Teixeira et al. (2017Teixeira AFS, Kemmelmeier K, Marascalchi MN, Stürmer SL, Carneiro MAC, Moreira FMS. 2017. Arbuscular mycorrhizal fungal communities in an iron mining area and its surroundings: Inoculum potential, density, and diversity of spores related to soil properties. Ciência e Agrotecnologia 41: 511-525.) and Vieira et al. (2018Vieira CK, Marascalchi MN, Rodrigues AV, Armas RD, Stürmer SL. 2018. Morphological and molecular diversity of arbuscular mycorrhizal fungi in revegetated iron-mining site has the same magnitude of adjacent pristine ecosystems. Journal of Environmental Sciences 67: 330-343.) in the Iron Quadrangle region in Minas Gerais. These authors detected 34 AMF species in 11 genera, with species belonging to Ambisporaceae, Pacisporaceae, Glomeraceae, Acaulosporaceae, and Gigasporaceae. Redundancy analyses showed that AMF communities were associated with organic matter in the dry season and Fe content in the soil in the rainy season, the latter being expected for a Canga soil (Vieira et al. 2018Vieira CK, Marascalchi MN, Rodrigues AV, Armas RD, Stürmer SL. 2018. Morphological and molecular diversity of arbuscular mycorrhizal fungi in revegetated iron-mining site has the same magnitude of adjacent pristine ecosystems. Journal of Environmental Sciences 67: 330-343.).
Richness and structure of AMF communities are affected by biotic factors such as host plant (Eom et al. 2000Eom AH, Hartnett DC, Wilson GWT. 2000. Host plant species effects on arbuscular mycorrhizal fungal communities in tallgrass prairie. Oecologia 122: 435-444.) and by several abiotic factors including fertilization (Lin et al. 2012Lin 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. Environment Science & Technology 46: 5764-5771. ), soil texture (Moebius-Clune et al. 2013Moebius-Clune DJ, Moebius-Clune BN, Van Es HM, Pawlowska TE. 2013. Arbuscular mycorrhizal fungi associated with a single agronomic plant host across the landscape: Community differentiation along a soil textural gradient. Soil Biology and Biochemistry 64: 191-199.), temperature and precipitation (Sun et al. 2013Sun XF, Su YY, 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. Chinese Science Bulletin 58: 4109-4119.), and fire (Gibson & Hetrick 1988Gibson DJ, Hetrick BAD. 1988. Topographic and fire effects on the composition and abundance of VA-mycorrhizal fungi in tallgrass prairie. Mycologia 80: 433-441.). Fire may have indirect or direct effects on AMF communities as it impacts plant community composition, soil temperature and water potential (Gibson & Hetrick 1988Gibson DJ, Hetrick BAD. 1988. Topographic and fire effects on the composition and abundance of VA-mycorrhizal fungi in tallgrass prairie. Mycologia 80: 433-441.). In Pakistan, burning decreased mycorrhizal inoculum potential in a scrub type of vegetation but it did not significantly alter AMF spore numbers and community composition (Rashid et al. 1997Rashid A, Ahmed T, Ayub N, Khan AG. 1997. Effect of forest fire on number, viability and post-fire re-establishment of arbuscular mycorrhizae. Mycorrhiza 7: 217-220.). In North American tallgrass prairies, burning episodes significantly decreased AMF species richness, increased total spore numbers, and affected species abundance differently (Eom et al. 1999Eom AH, Hartnett DC, Wilson GWT, Figge DAH. 1999. The effect of fire, mowing and fertilizer amendment on arbuscular mycorrhizas in tallgrass prairie. American Midland Naturalist 142: 55-70.). For instance, burning decreased the abundance of Glomus aggregatum but increased spore numbers of Claroideoglomus etunicatum and G. fecundisporum(Eom et al. 1999Eom AH, Hartnett DC, Wilson GWT, Figge DAH. 1999. The effect of fire, mowing and fertilizer amendment on arbuscular mycorrhizas in tallgrass prairie. American Midland Naturalist 142: 55-70.). In Mountain Chaco Forests of Argentina, burning affected spore density mainly by influencing species in Acaulosporaceae and Gigasporaceae, but not Glomeraceae (Longo et al. 2014Longo S, Nouhra E, Goto BT, Berbara RL, Urcelay C. 2014. Effects of fire on arbuscular mycorrhizal fungi in the Mountain Chaco Forest. Forest Ecology and Management 315: 86-94.). Overall, the effects of fire on AMF communities are hard to generalize, and responses differ in direction and magnitude due possibly to variation in fire characteristics (Longo et al. 2014Longo S, Nouhra E, Goto BT, Berbara RL, Urcelay C. 2014. Effects of fire on arbuscular mycorrhizal fungi in the Mountain Chaco Forest. Forest Ecology and Management 315: 86-94.).
Canga ecosystems occurring in the north region of Brazil in the Pará state are surrounded by evergreen tropical Amazonian rainforest in an environment not conducive to natural fires (Schmidt et al. 2018Schmidt IB, Moura LC, Ferreira MC, et al. 2018. Fire management in the Brazilian savanna: first steps and the way forward. The Journal of Applied Ecology 55: 2094-2101. ). Despite this, Canga vegetation in these regions suffers from occasional natural fires (Neves & Damasceno-Junior 2011Neves DRM, Damasceno-Junior GA. 2011. Post-fire phenology in a campo sujo vegetation in the Urucum plateau, Mato Grosso do Sul, Brazil. Revista Brasileira de Biologia 71: 881-888. ). In the Carajas Massif, a fire event was detected in an area of Canga, which set the stage to investigate this research on the effects of fire on mycorrhizal communities associated with ferruginous Canga vegetation. This work aimed to survey and compare species richness and taxonomic diversity of the AMF community occurring in burned and unburned areas of ferruginous Canga. We tested the hypothesis that burning decreases AMF spore number, species richness and mycorrhizal inoculum potential associated with Canga vegetation.
Materials and Methods
Study sites and sampling design
The study sites are located in the mineral province of Carajas, state of Pará, Brazil. The climate in the region is tropical, Aw according to Köppen’s classification (Alvares et al. 2013Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G. 2013. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22: 711-728.), with rainy summers and dry winters. Total annual rainfall is 1,827 mm and annual mean temperature is 26.2 oC. Soil samples were collected in October 2015 in two areas of ferruginous Canga: a native area with a recent history of natural burning in 2015 (BC, 06º 19’ 52’’ S, 49º 58’ 32’’ W) and a native area with no historic of burning (NC, 06º 23’ 47’’ S, 50º 22’ 31’’ W). These two areas were ca. 70 Km from each other. Both areas are within the Brazilian floristic domain Amazon Forest, which is part of the world biome Tropical and Subtropical Moist Broadleaf Forests.
In each area, three plots of 5 x 5 m each - adjacent to each other - were delimited during the dry season. From each of these plots, three distinct soil samples, 600-800 g each, were randomly obtained using a 6 cm wide soil corer or a shovel when soil was too shallow, resulting in three samples per plot and nine samples per area. Each sample was composed of three sub-samples obtained with the soil core which amounted for ca. 300 g of soil per sample. Soil samples were placed in plastic bags, and stored at 4 oC until processing.
Soil samples were thoroughly homogenized and an aliquot of 100 cm3 was used to extract and identify AMF spores and another aliquot of 200 cm3 was used for soil chemical analyses. A 200 cm3 subsample was obtained from each sample and pooled, which was used to establish trap cultures and to measure mycorrhizal inoculum potential for each area.
Soil chemical analyses
Soil chemical analyses were performed at the laboratory of Empresa de Pesquisa Agropecuária e Extensão Rural de Santa Catarina (EPAGRI, Chapecó, SC), following the methodology of Tedesco et al. (1995Tedesco MJ, Gianello C, Bissani CA, Bohnen H, Volkweiss SJ. 1995. Análise de solo, plantas e outros materiais. Boletim Técnico No 5. Porto Alegre, UFRGS.). Soil pH was measured in distilled water (1:1, vol/vol). Phosphorus (P) and K+ were extracted with HCl and H2SO4 while 1 M KCl was used to extract Ca2+, Mg2+, and Al3+. Organic matter content was measured by oxidation with a sulfochromic solution and determined using the Walkey-Black method described in Tedesco et al. (1995)Tedesco MJ, Gianello C, Bissani CA, Bohnen H, Volkweiss SJ. 1995. Análise de solo, plantas e outros materiais. Boletim Técnico No 5. Porto Alegre, UFRGS.. Data for soil chemical analyses are summarized in Table 1.
Chemical soil attributes of burned (BC) and unburned (NC) Canga areas from Pará state, Brazil. Values are means ± standard deviation (n = 9). CEC = Cation Exchange Capacity.
AMF spore extraction and identification
AMF spores were extracted from soil using wet sieving (Gerdemann & Nicolson 1963Gerdemann JW, Nicolson TH. 1963. Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Transactions of the British Mycological Society 46: 235-244.), followed by a sucrose gradient (20 %/60 %) centrifugation (Jenkins 1964Jenkins WR. 1964. A rapid centrifugal flotation technique for separating nematodes from soil. Plant Disease Report 48: 692.). Briefly, 100 cm3 of soil from each field sample were placed in a 2 L glass beaker, filled with tap water, and stirred using a glass rod. This soil suspension was poured onto nested sieves with 710 μm and 45 μm openings. Materials retained on the 710 μm sieve were removed and placed in a large Petri plate, and inspected under a dissecting microscope (Stemi 2000, Zeiss, Germany) for AMF sporocarps and spores attached to root pieces. Materials retained on the 45 μm sieve were transferred to 50 mL Falcon tubes containing the sucrose gradient and centrifuged at 700 × g for 1 minute. The supernatant was then poured over sieves with 300 μm, 180 μm, and 45 μm openings to facilitate spore separation by size, transferred to Petri plates and observed under a dissecting microscope. Spores were pulled out using an extruded glass pipette and separated by morphotype based on size, color, and shape. Spores were mounted on slides with PVLG (polyvinyl-alcohol lactoglycerol) and PVLG + Melzer’s reagent mixture (1:1, vol/vol) and identified under a microscope (Axiostar Plus, Zeiss, Germany). Identification was made by observing spore size, color, presence of ornamentation, spore wall structure, and Melzer’s reactions and comparing with original species descriptions and those found at web pages of the International Culture Collection of Arbuscular and Vesicular Arbuscular Mycorrhizal Fungi (INVAM - http://invam.caf.wvu.edu, West Virginia University, USA) and Blaszkowski (2012Blaszkowski J. 2012. Glomeromycota. W. Kraków, Safer Institute of Botany, Polish Academy of Sciences.). Classification at the family level adopted in this study follows that proposed by Redecker et al. (2013Redecker D, Schürler A, Stockinger H, Stürmer SL, Morton JB, Walker C. 2013. An evidence based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23: 515-531.).
The number of AMF species recovered in each area was used to measure species richness. Frequency of occurrence (F) was calculated as the number of samples that a given species was detected relative to the total number of soil samples per area and expressed as a percentage. Species were classified according to their frequency following Zhang et al. (2004Zhang Y, Gui LD, Liu RJ. 2004. Survey of arbuscular mycorrhizal fungi in deforested and natural forest land in the subtropical region of Dujiangyan, southwest China. Plant and Soil 261: 257-263.) as rare (F ≤ 10 %), common (10 % < F ≤ 30 %), most common (30 % < F ≤ 50 %), and dominant (F > 50 %).
Trap cultures
Trap cultures were established according to Stutz & Morton (1996Stutz JC, Morton JB. 1996. Successive pot cultures reveal high species richness of arbuscular endomycorrhizal fungi in arid ecosystems. Canadian Journal of Botany 74: 1883-1889.) to induce sporulation of AMF species that were not sporulating in the field at the sampling time. We established trap cultures for each area by mixing 600 g of field soil with 600 g of sterilized quartzite sand and placed in 1.5 kg plastic pots. Each pot received 40-60 seeds of brachiaria grass (Urochloa decumbens (Stapf) R.D. Webster) and plants were kept under greenhouse conditions. Plants were watered as needed and each pot received 100 mL of Hoagland’s nutrient solution without phosphorus after 60 days and with phosphorus after 120 days. After five months, a subsample of 100 cm3 was obtained to extract and identify AMF spores as described above. Part of the substrate of the first growth cycle was diluted with a soil:quartzite sand mix (1:1), in 1.5 kg pots and reseeded with brachiaria grass for a second 5-months growth cycle of trapping.
Mycorrhizal inoculum potential
The bioassay method of Moorman & Reeves (1979Moorman T, Reeves FB. 1979. The role of endomycorrhizae in revegetation practices in the semi-arid West. II. A bioassay to determine the effect of land disturbance on endomycorrhizal populations. American Journal of Botany 66: 14-18.) was used to estimate the mycorrhizal inoculum potential (MIP) for each area. For this bioassay, an aliquot (600 g) from the composite sample was diluted with a sterilized substrate (soil + quartzite sand, 1:1, vol/vol) and placed in 270 cm³ plastic cones. Four cones were established per area and seeded with brachiaria grass. Two seedlings were maintained per cone, and roots were sampled after 45 days, washed under tap water, and stained according to Koske & Gemma (1989Koske RE, Gemma JN. 1989. A modified procedure for staining roots to detect VA mycorrhizas. Mycological Research 92: 486-488.). The mycorrhizal inoculum potential for each area was measured by the percentage of mycorrhizal colonization assessed by the gridline intersect method of Giovannetti & Mosse (1980Giovannetti M, Mosse B. 1980. An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytologist 84: 489-500.).
Data analysis
Prior to statistical analyses, the total number of spores were transformed using log (x+1) and mycorrhizal colonization measured in the MIP bioassay transformed with arcsin square root (√%). A paired t-test was used to compare spore numbers, mycorrhizal colonization and species richness between areas. These procedures were made using the packages vegan (Oksanen et al. 2017Oksanen FJ, Blanchet G, Friendly M, et al. 2017. Vegan: Community Ecology Package. R package version 2.4-0. ) and packfor (Dray et al. 2016Dray S, Legendre P, Peres-Neto P. 2006. Spatial modelling: a comprehensive framework for principal сoordinate analysis of neighbour matrices (PCNM). Ecological Modelling 196: 483–493.) with R version 3.1.3 (R Core Team 2016R Core Team. 2016. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
https://www.R-project.org/...
).
Results
A total of 23 AMF species distributed in 10 genera and four families were detected in NC and BC from field-collected spores (Tab. 2). Gigasporaceae and Acaulosporaceae were represented by 11 and 8 species, respectively, and most species of Acaulosporaceae were found in both areas. Most species were classified as common, with their frequency ranging from 11 to 22 %, and no rare species were detected. Glomus sp1 and Acaulospora morrowiae were dominant species in both areas. Besides these two species, Acaulospora sp7 and Dentiscutata biornata in NC and Scutellospora sp9 and Bulbospora minima in BC were classified as dominant (Tab. 2). Twelve out of 23 species were shared between both areas.
Frequency of occurrence (F) of arbuscular mycorrhizal fungal species detected in burned (BC) and unburned (NC) Canga from Pará state, Brazil. Species within each area were categorized according to their frequency of occurrence as dominant (D), most common (MC), common (C), and rare (R).
Eight species sporulated in the first or second cycle of trap cultures, seven of them belonging to Gigasporaceae and one to Acaulosporaceae (Tab. 3). Species were detected in the first or second cycle of trap cultures only, except for D. biornata detected in both cycles. Gigaspora albida, Gigaspora gigantea, and Dentiscutata heterogama were detected exclusively from trap cultures.
Species of arbuscular mycorrhizal fungal species detected in trap cultures (1st and 2nd cycles) established with soils from burned (BC) and unburned (NC) Canga from Pará state, Brazil.
Total number of spores was 2.5 times higher in BC (1,442 ± 1,277) compared to NC (585 ± 302) but this difference was not significantly different (p > 0.05) (Fig. 1A). The number of species per sample ranged from 2 to 10 in BC and from 2 to 8 in NC, but the mean species richness was not significantly different between areas (Fig. 1B). Mycorrhizal colonization of U. decumbens in the inoculum potential bioassay did not differ significantly between areas and averaged 15.43 ± 6.08 and 12.58 ± 2.12 in BC and NC, respectively (Fig. 1C).
Total number of AMF spores (in 100 cm3 soil) (A), AMF species richness (B), and mycorrhizal colonization (%) measured in the infectivity bioassay (C) from areas of burned (BC) and unburned (NC) Canga. Means (bars) followed by the same letter are not significantly different (p ≤ 0.05).
Discussion
This study represents the first record of AMF communities associated with ferruginous Canga vegetation in the North region of Brazil, where the Amazon tropical rainforest surrounds this habitat. We used a fire event in a natural Canga area to examine the effect of burning on AMF species richness, spore numbers, and species richness. We recognize that the composition of AMF communities was investigated herein using solely morphological characters from spores recovered from field soils and trap cultures, with no attempt to use molecular methods. Although a molecular approach using amplicons from the large subunit (LSU) (Delavaux et al. 2022Delavaux CS, Ramos RJ, Stürmer SL, Bever JD. 2022. Environmental identification of arbuscular mycorrhizal fungi using the LSU rDNA gene region: an expanded database and improved pipeline. Mycorrhiza. doi: 10.1007/s00572-022-01068-3.
https://doi.org/10.1007/s00572-022-01068...
) and the small subunit (SSU) (Öpik et al. 2010Öpik M, Vanatoa A, Vanatoa E, et al. 2010. The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytologist 188: 223-241. ) rRNA genes may be desirable to investigate AMF community composition as complementary to the morphological approach, results published so far have shown that spore morphology can reveal most of the AMF species in a habitat (Wetzel et al. 2014Wetzel K, Silva GA, Matczinski U, Oehl F, Fester T. 2014. Superior differentiation of arbuscular mycorrhizal fungal communities from till and no-till plots by morphological spore identification when compared to T-RFLP. Soil Biology and Biochemistry 72: 88-96.; Vieira et al. 2018Vieira CK, Marascalchi MN, Rodrigues AV, Armas RD, Stürmer SL. 2018. Morphological and molecular diversity of arbuscular mycorrhizal fungi in revegetated iron-mining site has the same magnitude of adjacent pristine ecosystems. Journal of Environmental Sciences 67: 330-343.).
AMF communities in Canga were dominated by species of Acaulosporaceae and Gigasporaceae, which together accounted for 78 % of the total number of species recovered in NC and BC. Species of both families were also the only sporulators in trap cultures. Studies on soil factors that shape niche differentiation for AMF families indicate that soil pH and soil bulk density are key factors affecting the occurrence of Acaulosporaceae and Gigasporaceae (Lekberg et al. 2007Lekberg Y, Koide RT, Rohr JR, Aldrich-Wolfe L, Morton JB. 2007. Role of niche restrictions and dispersal in the composition of arbuscular mycorrhizal fungal communities. Journal of Ecology 95: 95-105.; Veresoglou et al. 2013Veresoglou SD, Caruso T, Rillig MC. 2013. Modelling the environmental and soil factors that shape the niches of two common arbuscular mycorrhizal fungal families. Plant and Soil 368: 507-518.). The probability of occurrence of Acaulosporaceae increased with high soil acidity and high soil bulk density (Veresoglou et al. 2013Veresoglou SD, Caruso T, Rillig MC. 2013. Modelling the environmental and soil factors that shape the niches of two common arbuscular mycorrhizal fungal families. Plant and Soil 368: 507-518.), while members of Gigasporaceae dominated sandy soils with high bulk density (Lekberg et al. 2007Lekberg Y, Koide RT, Rohr JR, Aldrich-Wolfe L, Morton JB. 2007. Role of niche restrictions and dispersal in the composition of arbuscular mycorrhizal fungal communities. Journal of Ecology 95: 95-105.). Both factors, acidic soils and high bulk density, are found in Canga soils, explaining the co-dominance of both AMF families found in this study. Soil pH in both areas studied herein ranged from 4.14 to 4.38 (Tab. 1), and it can be as low as 3.76 in Cangas from the Carajá region (Nunes 2009Nunes J. 2009. Floristica, estrutura e relações solo-vegetação em gradiente fitofisionômico sobre canga, na Serra Sul, FLONA de Carajás. MSc thesis. Universidade Federal de Viçosa, Viçosa. ). Soil bulk density is high in Canga compared with adjacent ecosystems, with values ranging from 1.25 to 1.62 g cm-3 (Tassinari 2015Tassinari D. 2015. Parâmetros físicos e mecânicos de solos em áreas alteradas pela mineração de ferro no município de Sabará, MG. MSc thesis, Universidade Federal de Lavras, Lavras.). Both families were also dominant in Canga habitats in Minas Gerais state, surveyed by Teixeira et al. (2017Teixeira AFS, Kemmelmeier K, Marascalchi MN, Stürmer SL, Carneiro MAC, Moreira FMS. 2017. Arbuscular mycorrhizal fungal communities in an iron mining area and its surroundings: Inoculum potential, density, and diversity of spores related to soil properties. Ciência e Agrotecnologia 41: 511-525.) and Vieira et al. (2018Vieira CK, Marascalchi MN, Rodrigues AV, Armas RD, Stürmer SL. 2018. Morphological and molecular diversity of arbuscular mycorrhizal fungi in revegetated iron-mining site has the same magnitude of adjacent pristine ecosystems. Journal of Environmental Sciences 67: 330-343.). It is interesting that Acaulosporaceae and Gigasporaceae dominated in Canga ecosystems from Minas Gerais and Pará (this study), separated by approximately 1,600 km. Although AMF community assemblages within a similar environment are largely unpredictable based on analyses of virtual taxa (Powell & Bennett 2015Powell JR, Bennett A. 2015. Unpredictable assembly of arbuscular mycorrhizal fungal communities. Pedobiologia 59: 11-15.), our results suggest that some predictability is possible at the family level for Canga vegetation due possibly to low soil pH and high bulk density. Gigasporaceae and Acaulosporaceae species have traits associated with competition and stress-tolerance, which would be favored in low P environments and in high soil acidity, all respectively (Chagnon et al. 2013Chagnon PL, Bradley RL, Maherali H, Klironomos JN. 2013. A trait-based framework to understand life history of mycorrhizal fungi. Trends in Plant Science 18: 484-491.). These traits could also explain the dominance of members of both families in Canga ecosystems that are depauperate in soil P and have low pH.
At the species level, we also observed some similarities between Cangas from Pará and Minas Gerais. First, most species identified herein were also present in Cangas from Minas Gerais, except Bulbospora minima, Racocetra fulgida, and Rhizophagus fasciculatum. Second, Acaulospora morrowiae, A. mellea, A. lacunosa and D. biornata were dominant and common AMF species in Cangas found in Pará (this study) and Minas Gerais (Teixeira et al. 2017Teixeira AFS, Kemmelmeier K, Marascalchi MN, Stürmer SL, Carneiro MAC, Moreira FMS. 2017. Arbuscular mycorrhizal fungal communities in an iron mining area and its surroundings: Inoculum potential, density, and diversity of spores related to soil properties. Ciência e Agrotecnologia 41: 511-525.; Vieira et al. 2018Vieira CK, Marascalchi MN, Rodrigues AV, Armas RD, Stürmer SL. 2018. Morphological and molecular diversity of arbuscular mycorrhizal fungi in revegetated iron-mining site has the same magnitude of adjacent pristine ecosystems. Journal of Environmental Sciences 67: 330-343.). All three Acaulospora species have been detected in four or more continents with a cosmopolitan distribution, while D. biornata has been detected in three continents (Stürmer et al. 2018Stürmer SL, Oliveira LZ, Morton JB. 2018. Gigasporaceae versus Glomeraceae (phylum Glomeromycota): A biogeographic tale of dominance in maritime sand dunes. Fungal Ecology 32: 49-56.), which explains their common occurrence in natural ecosystems. A common occurrence of these species suggests that these species are tolerant to the harsh environmental conditions found in Canga ecosystems, turning them into potential species to be used in revegetation programs of Canga. Our study expands the range of occurrence for some AMF species in brazilian floristic domains after the compilation of Maia et al. (2020Maia LC, Passos JH, Silva JÁ, Oehl F, Assis DMA. 2020. Species diversity of Glomeromycota in Brazilian biomes. Sydowia 72: 181-205.): Acaulospora lacunosa, Bulbospora minima, Racocetra fulgida, Gigaspora albida, and Gigaspora gigantea are the first report for the Brazilian Amazonian phytogeographic domain, contributing to the biogeography of these species.
We did not find evidence to support our hypothesis that fire would decrease AMF spore numbers, species richness and mycorrhizal inoculum potential in Canga soils. The total number of AMF spores was also not affected by fire in Araucaria forest (Moreira et al. 2006Moreira M, Baretta D, Tsai SM, Cardoso EJBN. 2006. Spore density and root colonization by arbuscular mycorrhizal fungi in preserved or disturbed Araucaria angustifolia (Bert.) O. Ktze. ecosystems. Scientia Agricola 63: 380-385. ), in temperate grasslands (Bentivenga & Hetrick 1992Bentivenga SP, Hetrick BAD. 1992. The effect of prairie management practices on mycorrhizal symbiosis. Mycologia 84: 522-527.; Eom et al. 1999Eom AH, Hartnett DC, Wilson GWT, Figge DAH. 1999. The effect of fire, mowing and fertilizer amendment on arbuscular mycorrhizas in tallgrass prairie. American Midland Naturalist 142: 55-70.), and mountain forests (Longo et al. 2014Longo S, Nouhra E, Goto BT, Berbara RL, Urcelay C. 2014. Effects of fire on arbuscular mycorrhizal fungi in the Mountain Chaco Forest. Forest Ecology and Management 315: 86-94.), but burning significantly decreased spore numbers in temperate forest sites (Vilariño & Arines 1991Vilariño A, Arines J. 1991. Numbers and viability of vesicular-arbuscular fungal propagules in field soil samples after wildfire. Soil Biology and Biochemistry 23: 1083-1087.). Fire could be perceived as a stress by AMF which could result in increasing sporulation if fire was severe. Our results suggest that the fire event experienced by the plant community in BC was not severe enough to trigger an increase in spore production by AMF species. Contrasting results are reported on the effect of fire upon mycorrhizal activity, with fire showing no significant effect on mycorrhizal inoculum potential in tallgrass prairie (Bentivenga & Hetrick 1992Bentivenga SP, Hetrick BAD. 1992. The effect of prairie management practices on mycorrhizal symbiosis. Mycologia 84: 522-527.) but decreased AMF propagule density (Vilariño & Arines 1991Vilariño A, Arines J. 1991. Numbers and viability of vesicular-arbuscular fungal propagules in field soil samples after wildfire. Soil Biology and Biochemistry 23: 1083-1087.). Although burning can raise soil temperature in a depth of up to 3-4 cm (Gibson & Hetrick 1988Gibson DJ, Hetrick BAD. 1988. Topographic and fire effects on the composition and abundance of VA-mycorrhizal fungi in tallgrass prairie. Mycologia 80: 433-441.), this might not be sufficient to affect spores and external mycelium. For instance, Barrett et al. (2014Barrett G, Campbell CD, Hodge A. 2014. The direct response of the external mycelium of arbuscular mycorrhizal fungi to temperature and the implications for nutrient transfer. Soil Biology and Biochemistry 78: 109-117.) observed that AMF external mycelium length of Glomus hoi and Rhizophagus intraradices was unaffected by increasing temperatures under experimental conditions. AMF spores are resting structures with relatively thick walls, and this feature might protect them from desiccation or structural changes that impair their viability and survival in soil. We had expected that mycorrhizal inoculum potential would decrease with fire since high temperatures would possibly affect AMF hyphae, which have thinner spore walls compared to spores. Although we did not measure whether hyphal length and activity decreased with burning, it is possible that spore numbers (which were not affected by burning) and colonized root fragments maintained mycorrhizal infectivity in Canga soils after burning. Our results suggest that AMF communities are resilient to a fire event in Canga as the total number of spores and mycorrhizal inoculum potential were of the same magnitude as that found in Canga with no history of burning.
Canga is a very fragile and threatened ecosystem that needs protection and restoration as it is directly affected by open cast iron mining. Taking advantage of a fire event, we demonstrated that AMF communities are not drastically affected by burning occurring in an area compared to areas with no history of burning. This suggests that AMF is an alternative to inoculate plants to be used in revegetation of areas in this ecosystem affected by natural burning. AMF community composition was similar in Cangas from the North region (this study) and those of the Southeast region (Teixeira et al. 2017Teixeira AFS, Kemmelmeier K, Marascalchi MN, Stürmer SL, Carneiro MAC, Moreira FMS. 2017. Arbuscular mycorrhizal fungal communities in an iron mining area and its surroundings: Inoculum potential, density, and diversity of spores related to soil properties. Ciência e Agrotecnologia 41: 511-525.; Vieira et al. 2018Vieira CK, Marascalchi MN, Rodrigues AV, Armas RD, Stürmer SL. 2018. Morphological and molecular diversity of arbuscular mycorrhizal fungi in revegetated iron-mining site has the same magnitude of adjacent pristine ecosystems. Journal of Environmental Sciences 67: 330-343.) of Brazil, which provides some baseline to identify and select AMF species to be used in programs of Canga revegetation and restoration. This study contributes to the biogeography of AMF in Brazilian floristics and the knowledge of soil biodiversity associated with Canga vegetation.
Acknowledgments
Authors thank the Instituto Tecnológico Vale (ITV) for the financial support to carry out field work in Canga areas and Antonio Eduardo Furtini Neto, Cecilio Frois Caldeira Jr., and Silvio Ramos for support during sampling. This study was supported by a grant from the Fundação de Amparo à Pesquisa e Inovação do Estado de Santa Catarina (grant FAPESC 2016TR2257) to SLS. KGHH thanks Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - CAPES, Brazil for a Doctoral assistantship (Finance Code 001). MNM thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for an undergraduate scientific research assistantship associated with PROTAX (Process 113.240/2016-3). SLS thanks the CNPq for a Research Assistantship (Process 307.995/2019-4). The authors are indebted to Camille Delavaux for comments and proofreading the manuscript and to two anonymous reviewers for their suggestions and comments.
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Publication Dates
-
Publication in this collection
29 July 2022 -
Date of issue
2022
History
-
Received
19 July 2021 -
Accepted
31 Mar 2022