Abstract
Fine root morphological traits and distribution, arbuscular mycorrhizal (AM) fungi, soil fertility, and nutrient concentration in fine root tissue were compared in sites under different successional phases: grass plants, secondary forest, and mature forest in Londrina county, Paraná state, southern Brazil. Soil cores were collected randomly at the 0–10- and 10–20-cm depths in three quadrants (50 m2) in each site. Plants from the different successional stages displayed high differences in fine root distribution, fine root traits, and mycorrhizal root colonization. There were increases in the concentration of nutrients both in soil and fine roots and decrease of bulk soil density along the succession. The fine root biomass and diameter increased with the succession progress. The total fine root length, specific root length, root hair length, and root hair incidence decreased with the succession advance. Similarly, the mycorrhizal root colonization and the density of AM fungi spores in the soil decreased along the succession. Mycorrhizal root colonization and spore density were positively correlated with fine root length, specific root length, root hair length, root hair incidence, and bulk density and negatively correlated with fine root diameter and concentration of some nutrients both in soil and root tissues. Nutrient concentration in root tissue and in soil was positively correlated with fine root diameter and negatively correlated with specific root length, root hair length, and root hair incidence. These results suggest different adaptation strategies of plant roots for soil exploration and mineral acquisition among the different successional stages. Early successional stages displayed plants with fine root morphology and AM fungi colonization to improve the root functional efficiencies for uptake of nutrients and faster soil resource exploration. Late successional stages displayed plants with fine root morphology and mycorrhizal symbiosis for both a lower rate of soil proliferation and soil exploration capacity to acquire nutrients.
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References
Abbott LK, Robson AD (1991) Factors influencing the occurrence of vesicular arbuscular mycorrhizas. Agric Ecosyst Environ 35:121–150 doi:10.1016/0167-8809(91)90048-3
Aidar MPM, Carrenho R, Joly CA (2004) Aspects of arbuscular mycorrhizal fungi in an Atlantic Forest chronosequence. Biota Neotropica 4:1–15
Allen EB, Rincon E, Allen MF, Perez-Jimenez A, Huante P (1998) Disturbance and seasonal dynamics of mycorrhizae in a tropical deciduous forest in Mexico. Biotropica 30:261–274 doi:10.1111/j.1744-7429.1998.tb00060.x
Baylis GTS (1975) The magnolioid mycorrhiza and mycotrophy in root systems derived from it. In: Sanders FE, Mosse B, Tinker PB (eds) Endomycorrhizas. Academic, New York, pp 373–389
Brown AM, Bledsoe C (1996) Spatial and temporal dynamics of mycorrhizas in Jaumea carnosa, a tidal salt marsh halophyte. J Ecol 84:703–715 doi:10.2307/2261333
Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304 doi:10.1046/j.1469-8137.2002.00397.x
Brundrett M (2004) Diversity and classification of mycorrhizal associations. Biol Rev Camb Philos Soc 79:473–495 doi:10.1017/S1464793103006316
Cavalheiro KO, Nepstad DC (1996) Deep soil heterogeneity and fine root distribution in forest and pastures of eastern Amazonia. Plant Soil 182:279–285
Cavelier J, Estevez J, Arjona B (1996) Fine root biomass in three successional stages of an Andean cloud forest in Colombia. Biotropica 28:728–736 doi:10.2307/2389059
Chagas e Silva F, Soares-Silva LH (2000) Arboreal flora of the Godoy Forest State Park, Londrina, PR. Brazil. Edinb J Bot 57:107–120 doi:10.1017/S096042860000007X
Coleman DC, Crossley DA Jr, Hendrix PF (2004) Fundamentals of soil ecology. Elsevier Academic, San Diego
Comas LH, Eissenstat DM (2004) Linking fine root traits to maximum potential growth rate among 11 mature temperate tree species. Funct Ecol 18:388–397 doi:10.1111/j.0269-8463.2004.00835.x
Comas LH, Bouma TJ, Eissenstat DM (2002) Linking root traits to potential growth rate in six temperate tree species. Oecologia 132:34–43 doi:10.1007/s00442-002-0922-8
Eissenstat DM (1992) Costs and benefits of constructing roots of small diameter. J Plant Nutr 15:763–782
Eissenstat DM, Wells CE, Yanai RD, Whitbeck JL (2000) Building roots in a changing environment: implications for root longevity. New Phytol 147:33–42 doi:10.1046/j.1469-8137.2000.00686.x
FAO (1994) Soil map of the world. FAO-UNESCO, Rome
Fischer CR, Janos DP, Perry DA, Linderman RG (1994) Mycorrhiza inoculum potentials in tropical secondary succession. Biotropica 26:369–377 doi:10.2307/2389230
Föehse D, Claassen N, Jungk A (1991) Phosphorus efficiency of plants II. Significance of root radius, root hairs and cation–anion balance for phosphorus influx in seven plant species. Plant Soil 132:261–271
Gahoonia TS, Nielsen NE (1998) Direct evidence on participation of root hairs in phosphorus (32P) uptake from soil. Plant Soil 198:147–152 doi:10.1023/A:1004346412006
Gahoonia TS, Nielsen NE, Joshi PA, Jahoor A (2001) A root hairless barley mutant for elucidating genetics of root hairs and phosphorus uptake. Plant Soil 235:211–219 doi:10.1023/A:1011993322286
Gamage HK, Singhakumara BMP, Ashton MS (2004) Effects of light and fertilization on arbuscular mycorrhizal colonization and growth of tropical rain-forest Syzygium tree seedlings. J Trop Ecol 20:525–534 doi:10.1017/S0266467404001592
Gange AC, Brown VK, Sinclair GS (1993) Vesicular–arbuscular mycorrhizal fungi: a determinant of plant community structure in early succession. Funct Ecol 7:616–622 doi:10.2307/2390139
Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular–arbuscular mycorrhizal infections in roots. New Phytol 84:489–500 doi:10.1111/j.1469-8137.1980.tb04556.x
Guariguata MR, Ostertag R (2001) Neotropical secondary forest succession: changes in structural and functional characteristics. For Ecol Manage 148:185–206 doi:10.1016/S0378-1127(00)00535-1
Guo DL, Mitchell RJ, Hendricks JJ (2004) Fine root branch orders respond differentially to carbon source-sink manipulations in a longleaf pine forest. Oecologia 140:450–457 doi:10.1007/s00442-004-1596-1
Hendrick RL, Pregitzer KS (1996) Temporal and depth-related patterns of fine root dynamics in northern hard wood forests. J Ecol 84:167–176 doi:10.2307/2261352
Hetrick BAD, Wilson GWT, Todd TC (1992) Relationships of mycorrhizal symbiosis, root strategy, and phenology among tallgrass prairie forbs. Can J Bot 70:1521–1528 doi:10.1139/b92-253
Hinsinger P, Gobran GR, Gregory PJ, Wenzel WW (2005) Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes. New Phytol 168:293–303 doi:10.1111/j.1469-8137.2005.01512.x
Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162:9–24 doi:10.1111/j.1469-8137.2004.01015.x
Ingleby K, Diagne O, Deans JD, Lindley DK, Neyra M, Ducousso M (1997) Distribution of roots, arbuscular mycorrhizal colonization and spores around fast-growing tree species in Senegal. For Ecol Manage 90:19–27 doi:10.1016/S0378-1127(96)03875-3
Itoh S, Barber SA (1983) Phosphorus uptake by six plant species as related to root hairs. Agron J 75:457–461
Jackson RB, Mooney HA, Schulze ED (1997) A global budget for fine root biomass, surface area, and nutrient contents. Proc Natl Acad Sci USA 94:7362–7366 doi:10.1073/pnas.94.14.7362
Jasper DA, Abbott LK, Robson AD (1991) The effect of soil disturbance on vesicular–arbuscular mycorrhizal fungi in soils from different vegetation types. New Phytol 118:471–476 doi:10.1111/j.1469-8137.1991.tb00029.x
Lusk CH, Reich PB, Montgomery RA, Ackerly DD, Cavender-Bares J (2008) Why are evergreen leaves so contrary about shade? Trends Ecol Evol 23:299–303 doi:10.1016/j.tree.2008.02.006
Lynch JP, Ho MD (2005) Rhizoeconomics: carbon costs of phosphorus acquisition. Plant Soil 269:45–56 doi:10.1007/s11104-004-1096-4
Manjunath A, Habte M (1991) Root morphological characteristics of host species having distinct mycorrhizal dependency. Can J Bot 69:671–676 doi:10.1139/b91-089
Marschner H (1998) Role of root growth, arbuscular mycorrhiza, and root exudates for the efficiency in nutrient acquisition. Field Crops Res 56:203–207 doi:10.1016/S0378-4290(97)00131-7
Matsumoto LS, Martines AM, Avanzi MA, Albino UB, Brasil CB, Saridakis DP et al (2005) Interactions among functional groups in the cycling of, carbon, nitrogen and phosphorus in the rhizosphere of three successional species of tropical woody trees. Appl Soil Ecol 28:57–65 doi:10.1016/j.apsoil.2004.06.008
McGonigle TP, Evans DG, Miller MH (1990) Effect of degree of soil disturbance on mycorrhizal colonization and phosphorus absorption by maize in growth chamber and field experiments. New Phytol 116:629–636 doi:10.1111/j.1469-8137.1990.tb00548.x
Muthukumar T, Sha L, Yang X, Cao M, Tang J, Zheng Z (2003) Distribution of roots and arbuscular mycorrhizal associations in tropical forest types of Xishuangbanna, southwest China. Appl Soil Ecol 22:241–253 doi:10.1016/S0929-1393(02)00156-7
Newsham KK, Fitter AH, Watkinson AR (1995) Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends Ecol Evol 10:407–411 doi:10.1016/S0169-5347(00)89157-0
Nielsen KL, Bouma TJ, Lynch JP, Eissenstat DM (1998) Effects of phosphorus availability and vesicular–arbuscular mycorrhizas on the carbon budget of common bean (Phaseolus vulgaris). New Phytol 139:647–656 doi:10.1046/j.1469-8137.1998.00242.x
Phillips JM, Hayman DS (1970) Improved procedures for clearing roots for rapid assessment of infection. Trans Br Mycol Soc 55:158–161
Picone C (2000) Diversity and abundance of arbuscular-mycorrhizal fungus spores in tropical forest and pasture. Biotropica 32:734–750 doi:10.1646/0006-3606(2000)032[0734:DAAOAM]2.0.CO;2
Powers JS, Treseder KK, Lerdau MT (2005) Fine roots, arbuscular mycorrhizal hyphae and soil nutrients in four neotropical rain forests: patterns across large geographic distance. New Phytol 165:913–921 doi:10.1111/j.1469-8137.2004.01279.x
Rabatin SC, Stinner BR (1988) Indirect effects of interactions between VAM fungi and soil-inhabiting invertebrates on plant processes. Agric Ecosyst Environ 24:135–146 doi:10.1016/0167-8809(88)90061-8
Raghothama KG, Karthikeyan AS (2005) Phosphate acquisition. Plant Soil 274:37–49 doi:10.1007/s11104-004-2005-6
Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems—a journey towards relevance? New Phytol 157:475–492 doi:10.1046/j.1469-8137.2003.00704.x
Röderstein M, Hertel D, Leuschner C (2005) Above- and below-ground litter production in three tropical montane forests in southern Ecuador. J Trop Ecol 21:483–492 doi:10.1017/S026646740500249X
Schweiger PF, Robson AD, Barrow N (1995) Root hair length determines beneficial effect of a Glomus species on shoot growth of some pasture species. New Phytol 131:247–254 doi:10.1111/j.1469-8137.1995.tb05726.x
Sieverding E (1991) Vesicular arbuscular mycorrhiza management in tropical agrosystems. Deutsche Gesellschaft für Technische Zusammenarbeit (GTZ) GmbH, Eschbon
Siqueira JO, Saggin-Júnior OJ (2001) Dependency on arbuscular mycorrhizal fungi and responsiveness of some Brazilian native woody species. Mycorrhiza 11:245–255 doi:10.1007/s005720100129
Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, London
Stürmer SL, Klauberg Filho O, Queiroz MH, Mendonça MM (2006) Occurrence of arbuscular mycorrhizal fungi in soils of early stages of a secondary succession of Atlantic Forest in South Brazil. Acta Bot Brasilica 20:513–521
Tennant D (1975) A test of modified line intersect method estimating root length. J Ecol 63:995–1001 doi:10.2307/2258617
Tilman D (1994) Competition and biodiversity in spatially structured habitats. Ecology 75:2–16 doi:10.2307/1939377
Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355 doi:10.1111/j.1469-8137.2004.01159.x
Vitousek PM (1984) Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology 65:285–298 doi:10.2307/1939481
Wright IJ, Westoby M (1999) Differences in seedling growth behavior among species: trait correlations across species, and trait shifts along nutrient compared to rainfall gradients. J Ecol 87:85–97 doi:10.1046/j.1365-2745.1999.00330.x
Zangaro W, Andrade G (2002) Micorrizas arbusculares em espécies arbóreas nativas da bacia do rio Tibagi. In: Medri ME, Bianchini E, Pimenta JA, Shibata O (eds) A bacia do rio Tibagi. Edição dos editores, Londrina, pp 171–210
Zangaro W, Bononi VLR, Trufen SB (2000) Mycorrhizal dependency, inoculum potential and habitat preference of native woody species in South Brazil. J Trop Ecol 16:603–622 doi:10.1017/S0266467400001607
Zangaro W, Nisizaki SMA, Domingos JCB, Nakano EM (2003) Mycorrhizal response and successional status in 80 woody species from south Brazil. J Trop Ecol 19:315–324 doi:10.1017/S0266467403003341
Zangaro W, Nishidate FR, Camargo FRS, Romagnoli GG, Vandresen J (2005) Relationships among arbuscular mycorrhizas, root morphology and seedling growth of tropical native woody species in southern Brazil. J Trop Ecol 21:529–540 doi:10.1017/S0266467405002555
Zangaro W, Nishidate FR, Vandresen J, Andrade G, Nogueira MA (2007) Root mycorrhizal colonization and plant responsiveness are related to root plasticity, soil fertility and successional status of native woody species in southern Brazil. J Trop Ecol 23:53–62 doi:10.1017/S0266467406003713
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Zangaro, W., de Assis, R.L., Rostirola, L.V. et al. Changes in arbuscular mycorrhizal associations and fine root traits in sites under different plant successional phases in southern Brazil. Mycorrhiza 19, 37–45 (2008). https://doi.org/10.1007/s00572-008-0202-5
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DOI: https://doi.org/10.1007/s00572-008-0202-5