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Succession and environmental variation influence soil exploration potential by fine roots and mycorrhizal fungi in an Atlantic ecosystem in southern Brazil

Published online by Cambridge University Press:  10 March 2014

Waldemar Zangaro ,
Ricardo de Almeida Alves ,
Priscila Bochi de Souza ,
Leila Vergal Rostirola ,
Luiz Eduardo Azevedo Marques Lescano ,
Artur Berbel Lírio Rondina  and
Marco Antonio Nogueira
Waldemar Zangaro*
Affiliation:
Universidade Estadual de Londrina, Centro de Ciências Biológicas, Departamento de Biologia Animal e Vegetal, 86051-990, Londrina, PR, Brazil Programa de Pós-Graduação em Ciências Biológicas, Departamento de Biologia Animal e Vegetal, Universidade Estadual de Londrina, PR, Brazil
Ricardo de Almeida Alves
Affiliation:
Universidade Estadual de Londrina, Centro de Ciências Biológicas, Departamento de Biologia Animal e Vegetal, 86051-990, Londrina, PR, Brazil Programa de Pós-Graduação em Ciências Biológicas, Departamento de Biologia Animal e Vegetal, Universidade Estadual de Londrina, PR, Brazil
Priscila Bochi de Souza
Affiliation:
Universidade Estadual de Londrina, Centro de Ciências Biológicas, Departamento de Biologia Animal e Vegetal, 86051-990, Londrina, PR, Brazil
Leila Vergal Rostirola
Affiliation:
Universidade Estadual de Londrina, Centro de Ciências Biológicas, Departamento de Biologia Animal e Vegetal, 86051-990, Londrina, PR, Brazil
Luiz Eduardo Azevedo Marques Lescano
Affiliation:
Universidade Estadual de Londrina, Centro de Ciências Biológicas, Departamento de Biologia Animal e Vegetal, 86051-990, Londrina, PR, Brazil Programa de Pós-Graduação em Microbiologia, Departamento de Microbiologia, Universidade Estadual de Londrina, PR, Brazil
Artur Berbel Lírio Rondina
Affiliation:
Universidade Estadual de Londrina, Centro de Ciências Biológicas, Departamento de Biologia Animal e Vegetal, 86051-990, Londrina, PR, Brazil Programa de Pós-Graduação em Ciências Biológicas, Departamento de Biologia Animal e Vegetal, Universidade Estadual de Londrina, PR, Brazil
Marco Antonio Nogueira
Affiliation:
Programa de Pós-Graduação em Microbiologia, Departamento de Microbiologia, Universidade Estadual de Londrina, PR, Brazil Embrapa Soja, PO Box 231, 86001-970, Londrina, PR, Brazil
*
1 Corresponding author. Email: [email protected]
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Abstract:

Fast-growing plant species are plentiful at the early stages of succession and possess roots with greater capacity for soil exploration than slow-growing plant species of late stages. Thus, the dynamics of fine-root production, morphological traits and arbuscular mycorrhizal fungal (AMF) infection intensity were assessed monthly over 1 y in the grassland, scrub, secondary and mature forests of the Atlantic Forest ecosystem, amounting to 13 consecutive samplings. Fine roots were sampled in three 100 × 100-m plots at each study site. Each plot was subdivided in five 20 × 100-m subplots and 15 soil samples were randomly taken from a depth of 0–5 cm in soil within each plot. The average of the fine-root dry mass increased from 1.39 mg cm−3 soil in the grassland to 3.37 mg cm−3 in the secondary forest; fine-root tip diameter varied from 146 μm in the grassland to 303 μm in the mature forest; tissue density from 0.24 g cm−3 root in the grassland to 0.30 g cm−3 in the mature forest and fine-root length was 4.52 cm cm−3 soil in the grassland and 6.48 cm cm−3 soil in the secondary forest. On the other hand, fine-root specific length decreased from 43.9 m g−1 root to 18.3 m g−1 root in the mature forest; incidence of root hairs was 67% in the grassland and 30% in the mature forest; the length of root hairs was 215 μm in the grassland and 112 μm in the mature forest; and the intensity of AMF infection decreased from 66% in the grassland to 17% in the mature forest. In addition to AMF infection, the environmental variation also affected dry mass production and morphological traits of fine roots. During the cool season, fine-root dry mass, fine-root length, incidence and length of root hairs and intensity of AMF infection decreased compared with the warm season. We verified that the potential for soil exploration, that expresses the capacity for nutrient acquisition via fine roots and AMF infection intensity, decreased during the cool season and with the advance of the successional groups. These results indicate that fine-root traits and intensity of AMF infection are influenced by the intrinsic nutrient requirements of the plant species in each ecological group.

Keywords

arbuscular mycorrhizal fungicarbon economynutrient acquisitionroot dynamicssoil fertilitytropical forest
Type
Research Article
Information
Journal of Tropical Ecology , Volume 30 , Issue 3 , May 2014 , pp. 237 - 248
Copyright
Copyright © Cambridge University Press 2014 

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References

LITERATURE CITED

AIDAR, M. P. M., CARRENHO, R. & JOLY, C. A. 2004. Aspects of arbuscular mycorrhizal fungi in an Atlantic Forest chronosequence. Biota Neotropica 4:1–15.Google Scholar
BATES, T. R. & LYNCH, J. P. 2001. Root hairs confer a competitive advantage under low phosphorus availability. Plant and Soil 236:243–250.CrossRefGoogle Scholar
BROWN, S. & LUGO, A. E. 1994. Rehabilitation of tropical lands: a key to sustaining development. Restoration Ecology 2:97–111.Google Scholar
BRUNDRETT, M., BEEGHER, N., DELL, B., GROOVE, T. & MALAJCZUK, N. 1996. Working with mycorrhizas in forestry and agriculture. ACIAR Monograph, Canberra. 374 pp.Google Scholar
CAIRNS, M. A., BROWN, S., HELMER, E. H. & BAUMGARDNER, G. A. 1997. Root biomass allocation in the world's upland forests. Oecologia 111:1–11.Google Scholar
CAVALHEIRO, K. O. & NEPSTAD, D. C. 1996. Deep soil heterogeneity and fine root distribution in forest and pastures of eastern Amazonia. Plant and Soil 182:279–285.Google Scholar
CAVELIER, J., ESTEVES, J. & ARJONA, B. 1996. Fine root biomass in three successional stages of an Andean cloud forest in Colombia. Biotropica 28:728–736. Google Scholar
CHAGAS E SILVA, F. & SOARES-SILVA, L. H. 2000. Arboreal flora of the Godoy Forest State Park, Londrina, PR. Brazil. Edinburgh Journal of Botany 57:107–120.Google Scholar
CHEN, X., EAMUS, D. & HUTLEY, L. B. 2004. Seasonal patterns of fine-root productivity and turnover in a tropical savanna of northern Australia. Journal of Tropical Ecology 20:221–224.CrossRefGoogle Scholar
COMAS, L. H. & EISSENSTAT, D. M. 2004. Linking fine root traits to maximum potential growth rate among 11 mature temperate tree species. Functional Ecology 18:388–397.Google Scholar
COMAS, L. H., BOUMA, T. J. & EISSENSTAT, D. M. 2002. Linking root traits to potential growth rate in six temperate tree species. Oecologia 132:34–43.Google Scholar
COMAS, L. H., MUELLER, K. E., TAYLOR, L. L., MIDFORD, P. E., CALLAHAN, H. S. & BEERLING, D. J. 2012. Evolutionary patterns and biogeochemical significance of angiosperm root traits. International Journal of Plant Sciences 173:584–595.CrossRefGoogle Scholar
DRESS, W. J. & BOERNER, R. E. J. 2001. Root dynamics of southern Ohio oak-hickory forests influences of prescribed fire and landscape position. Canadian Journal of Forest Research 31:644–653.Google Scholar
EISSENSTAT, D. M. 1992. Costs and benefits of constructing roots of small diameter. Journal of Plant Nutrition 15:763–782.Google Scholar
EISSENSTAT, D. M. & YANAI, R. D. 1997. The ecology of root life span. Advances in Ecological Research 27:1–62.Google Scholar
EISSENSTAT, D. M., WELLS, C. E., YANAI, R. D. & WHITBECK, J. L. 2000. Building roots in a changing environment: implications for root longevity. New Phytologist 147:33–42.Google Scholar
FITTER, A. H., GRAVES, J. D., SELF, G. K., BROWN, T. K., BOGIE, D. S. & TAYLOR, K. 1998. Root production, turnover and respiration under two grassland types along an altitudinal gradient: influence of temperature and solar radiation. Oecologia 114:20–30.CrossRefGoogle ScholarPubMed
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 and Soil 132:261–271.Google Scholar
FOOD AND AGRICULTURE ORGANIZATION (FAO). 1994. Soil map of the world. FAO-UNESCO, Rome.Google Scholar
GAHOONIA, T. S., NIELSEN, N. E., JOSHI, P. A. & JAHOOR, A. 2001. A root hairless barley mutant for elucidating genetics of root hairs and phosphorus uptake. Plant and Soil 235:211–219.CrossRefGoogle Scholar
GAMAGE, H. K., SINGHAKUMARA, B. M. P. & ASHTON, M. S. 2004. Effects of light and fertilization on arbuscular mycorrhizal colonization and growth of tropical rain-forest Syzygium tree seedlings. Journal of Tropical Ecology 20:525–534.Google Scholar
GIOVANNETTI, M., SBRANA, C., CITERNESI, A. S. & AVIO, L. 1996. Analysis of factors involved in fungal recognition responses to host derived signals by arbuscular mycorrhizal fungi. New Phytologist 133:65–71.CrossRefGoogle Scholar
GOWER, S. T. 1987. Relations between mineral nutrient availability and fine root biomass in two Costa Rican tropical wet forests: a hypothesis. Biotropica 19:171–175.CrossRefGoogle Scholar
GUADARRAMA, P. & ALVAREZ-SANCHEZ, F. J. 1999. Abundance of arbuscular mycorrhizal fungi spores in different environments in a tropical rain forest, Veracruz, Mexico. Mycorrhiza 8:267–270.Google Scholar
GUARIGUATA, M. R. & OSTERTAG, R. 2001. Neotropical secondary forest succession: changes in structural and function characteristics. Forest Ecology and Management 148:185–206.Google Scholar
HENDRICK, R. L. & PREGITZER, K. S. 1996. Applications of minirhizotrons to understand root function in forests and other natural ecosystems. Plant and Soil 185:293–304.Google Scholar
HERTEL, D., LEUSCHNER, C. & HÖLSCHER, D. 2003. Size and structure of fine root systems in old-growth and secondary tropical montane forests (Costa Rica). Biotropica 35:143–153.Google Scholar
HODGE, A. 2004. The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytologist 162:9–24.CrossRefGoogle Scholar
HOLDAWAY, R. J., RICHARDSON, S. J., DICKIE, I. A., PELTZER, D. A. & COOMES, D. A. 2011. Species- and community-level patterns in fine root traits along a 120000-year soil chronosequence in temperate rain forest. Journal of Ecology 99:954–963.Google Scholar
HUANTE, P., RINCON, E. & ALLEN, E. B. 1993. Effect of vesicular-arbuscular mycorrhizae on seedling growth of four tree species from the tropical deciduous forest in Mexico. Mycorrhiza 2:141–145.CrossRefGoogle Scholar
ITOH, S. & BARBER, S. A. 1983. Phosphorus uptake by six plant species as related to root hairs. Agronomic Journal 75:457–461.Google Scholar
JANOS, D. P. 1980. Mycorrhizae influence tropical succession. Biotropica 12:56–64.Google Scholar
JANOS, D. P. 1983. Tropical mycorrhizas, nutrient cycles and plant growth. Pp. 327–345 in Sutton, S. L., Whitmore, T. C. & Chadwick, A. C. (eds.). Tropical rain forest: ecology and management. Blackwell Scientific Publications, Oxford.Google Scholar
JARAMILLO, V. J., AHEDO-HERNÁNDEZ, R. & KAUFFMAN, J. B. 2003. Root biomass and carbon in a tropical evergreen forest of Mexico: changes with secondary succession and forest conversion to pasture. Journal of Tropical Ecology 19:457–464.Google Scholar
LACERDA, K. A. P., SILVA, M. M. S., CARNEIRO, M. A. C., REIS, E. F. & SAGGIN JÚNIOR, O. J. 2011. Fungos micorrízicos arbusculares e adubação fosfatada no crescimento inicial de seis espécies arbóreas do cerrado. Cerne 17:377–386.Google Scholar
LUSK, C. H., REICH, P. B., MONTGOMERY, R. A., ACKERLY, D. D. & CAVENDER-BARES, J. 2008. Why are evergreen leaves so contrary about shade? Trends in Ecology and Evolution 23:299–303.Google Scholar
MATSUMOTO, L. S., MARTINES, A. M., AVANZI, M. A., ALBINO, U. B., BRASIL, C. B., SARIDAKIS, D. P., RAMPAZO, L. G. L., ZANGARO, W. & ANDRADE, G. 2005. Interactions among functional groups in the cycling of carbon, nitrogen and phosphorus in the rhizosphere of three successional species of tropical woody trees. Applied Soil Ecology 28:57–65.Google Scholar
MAYCOCK, C. R. & CONGDON, R. A. 2000. Fine root biomass and soil N and P in north Queensland rain forests. Biotropica 32:185–190.Google Scholar
MCGONIGLE, T. P., EVANS, D. G. & MILLER, M. H. 1990. Effect of degree of soil disturbance on mycorrhizal colonization and phosphorus absortion by maize in growth chamber and field experiments. New Phytologist 116:629–636.Google Scholar
MCMICHAEL, B. L. & BURKE, J. J. 1998. Soil temperature and root growth. HortScience 33:947–951.Google Scholar
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. Applied Soil Ecology 22:241–253.Google Scholar
NIELSEN, K. L., BOUMA, T. J., LYNCH, J. P. & EISSENSTAT, D. M. 1998. Effects of phosphorus availability and vesicular–arbuscular mycorrhizas on the carbon budget of common bean (Phaseolus vulgaris). New Phytologist 139:647–656.Google Scholar
NORBY, R. J. & JACKSON, R. B. 2000. Root dynamics and global change: seeking an ecosystem perspective. New Phytologist 147:3–12.Google Scholar
POWERS, J. S., TRESEDER, K. K. & LERDAU, M. T. 2005. Fine roots, arbuscular mycorrhizal hyphae and soil nutrients in four neotropical rain forests: patterns across large geographic distance. New Phytologist 165:913–921.CrossRefGoogle Scholar
REICH, P. B., TJOELKER, M. G., WALTERS, M. B., VANDERKLEIN, D. W. & BUSCHENA, C. 1998. Close association of RGR, leaf and root morphology, seed mass and shade tolerance in seedlings of nine boreal tree species grown in high and low light. Functional Ecology 12:327–338.CrossRefGoogle Scholar
ROBINSON, D., HODGE, A. & FITTER, A. H. 2003. Constraints on the form and function of root systems. Pp. 1–31 in Kroon, H. & Visser, E. J. W. (eds.). Root ecology. Ecological Studies(v. 168), Springer-Verlag, Berlin.Google Scholar
RYSER, P., & LAMBERS, H. 1995. Root and leaf attributes accounting for the performance of fast- and slow-growing grasses at different nutrient supply. Plant and Soil 170:251–265.CrossRefGoogle Scholar
SIQUEIRA, J. O., CARNEIRO, M. A. C., CURI, N., ROSADO, S. C. S. & DAVIDE, A. C. 1998. Mycorrhizal colonization and mycotrophic growth of native woody species as related to successional groups in southeastern Brazil. Forest Ecology and Management 107:241–252.Google Scholar
SON, Y. & HWANG, J. H. 2003. Fine root biomass, production and turnover in a fertilized Larix leptolepis plantation in central Korea. Ecological Research 18:339–346.Google Scholar
TENNANT, D. A. 1975. Test of a modified line intersect method of estimating root length. Journal of Ecology 63:995–1001.Google Scholar
TER BRAAK, C. J. F. & SMILAUER, P. 1988. CANOCO Reference Manual and User's Guide to Canoco for Windows: Software for Canonical Community Ordination (Version 4). Microcomputer Power, Ithaca. 352 pp.Google Scholar
VANDRESEN, J., NISHIDATE, F. R., TOREZAN, J. M. D. & ZANGARO, W. 2007. Inoculação de fungos micorrízicos arbusculares e adubação na formação e pós-transplante de mudas de cinco espécies arbóreas nativas do sul do Brasil. Acta Botanica Brasilica 21:753–765.CrossRefGoogle Scholar
VOGT, K. A., VOGT, D. J., PALMIOTTO, P. A., BOON, P., O‘HARA, J. & ASBJORNSEN, H. 1996. Review of root dynamics in forest ecosystems groups by climate, climatic forest type and species. Plant and Soil 187:159–219.Google Scholar
WRIGHT, I. J. & WESTOBY, M. 1999. Differences in seedling growth behavior among species: trait correlations across species, and trait shifts along nutrient compared to rainfall gradients. Journal of Ecology 87:85–97.Google Scholar
ZANGARO, W. & MOREIRA, M. 2010. Micorrizas arbusculares nos biomas floresta atlântica e floresta de araucária. Pp. 279–310 in Siqueira, J. O., Souza, F. A., Cardoso, E. J. B. N. & Tsai, S. M. (eds). Micorrizas: trinta anos de pesquisa no Brasil. Editora UFLA, Brasília.Google Scholar
ZANGARO, W., BONONI, V. L. R. & TRUFEN, S. B. 2000. Mycorrhizal dependency, inoculum potential and habitat preference of native woody species in South Brazil. Journal of Tropical Ecology 16:603–622.Google Scholar
ZANGARO, W., NISIZAKI, S. M. A., DOMINGOS, J. C. B. & NAKANO, E. M. 2003. Mycorrhizal response and sucessional status in 80 woody species from south Brazil. Journal of Tropical Ecology 19:315–324.CrossRefGoogle Scholar
ZANGARO, W., NISHIDATE, F. R., CAMARGO, F. R. S., ROMAGNOLI, G. G. & VANDRESEN, J. 2005. Relationships among arbuscular mycorrhizas, root morphology and seedling growth of tropical native woody species in southern Brazil. Journal of Tropical Ecology 21:529–540.Google Scholar
ZANGARO, W., ANDRADE, G., NOGUEIRA, M. A., NISHIDATE, F. R. & VANDRESEN, J. 2007. Relation among soil fertility, arbuscular mycorrhizas and root morphology in the growth of 12 successional native woody species from the south of Brazil. Journal of Tropical Ecology 23:53–62.Google Scholar
ZANGARO, W., ASSIS, R. L., ROSTIROLA, L. V., SOUZA, P. B., GONÇALVES, M. C., ANDRADE, G. & NOGUEIRA, M. A. 2008. Changes in arbuscular mycorrhizal associations and fine root traits in sites under different plant successional phases in southern Brazil. Mycorrhiza 19:37–45.Google Scholar
ZANGARO, W., ALVES, R. A., LESCANO, L. E. A. M., ANSANELO, A. P. & NOGUEIRA, M. A. 2012 a. Investment in fine roots and arbuscular mycorrhizal fungi decrease during succession in three Brazilian ecosystems. Biotropica 44:141–150.Google Scholar
ZANGARO, W., ANSANELO, A. P., LESCANO, L. E. A. M., ALVES, R. A., RONDINA, A. B. L. & NOGUEIRA, M. A. 2012 b. Infection intensity, spore density and inoculum potential of arbuscular mycorrhizal fungi decrease during secondary succession in tropical Brazilian ecosystems. Journal of Tropical Ecology 28:453–462.CrossRefGoogle Scholar
ZANGARO, W., ROSTIROLA, L. V., SOUZA, P. B., ALVES, R. A., LESCANO, L. E. A. M., RONDINA, A. B. L., NOGUEIRA, M. A. & CARRENHO, R. 2013. Root colonization and spore abundance of arbuscular mycorrhizal fungi in distinct successional stages from an Atlantic rainforest biome in southern Brazil. Mycorrhiza 23:221–233.Google Scholar