Hostname: page-component-848d4c4894-x24gv Total loading time: 0 Render date: 2024-05-13T19:48:08.840Z Has data issue: false hasContentIssue false

Differences between root traits of early- and late-successional trees influence below-ground competition and seedling establishment

Published online by Cambridge University Press:  13 June 2016

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
Luis Eduardo Azevedo Marques Lescano
Affiliation:
Universidade Estadual do Norte do Paraná, Campus Luiz Meneghel, 86360-000, Bandeirantes, PR, Brazil
Enio Massao Matsuura
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
Artur Berbel Lirio 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:
Embrapa Soja, PO Box 231, 86001–970, Londrina, PR, Brazil Programa de Pós-Graduação em Microbiologia, Departamento de Microbiologia, Universidade Estadual de Londrina, PR, Brazil
*
1Corresponding author. Email: wzangaro@uel.br

Abstract:

The competitive influence of the root system of the exotic grass Urochloa brizantha and the widespread forb Leonotis nepetifolia on the emergence, survival and early growth of the seedlings of eight tropical heliophilous herbaceous species, six early-successional woody species and five late-successional woody species from Brazil, grown in 3500-cm3 pots and in greenhouse without light restriction were assessed. The density of fine-root systems produced by the forb and the grass in pots were 6.8 cm cm−3 soil and 48.1 cm cm−3 soil, respectively. Seedlings survival of the heliophilous herbaceous, early- and late-successional woody species were 86%, 70% and 100% in presence of the forb root system and 12%, 14% and 100% in competition with grass root system, respectively. The competitive pressure applied by the grass root system on seedling growth of the heliophilous herbaceous, early- and late-successional woody species were 2.4, 1.9 and 1.4 times greater than the forb root system. Total root length of the heliophilous herbaceous, early- and late-successional woody species grown without competitors were 13, 33 and 5 times greater than in competition with forb, and were 66, 54 and 6 times greater than in competition with grass root system, respectively. The averages of fine-root diameter of plants grown without competitors were 209 μm for the heliophilous herbaceous, 281 μm for early-successional trees and 382 μm for late-successional trees. The root system of the forb did not avoid seedling establishment of most plant species, but the grass root system hampered more the establishment of heliophilous herbaceous and early-successional woody species than the seedling establishment of late-successional woody species. The different density of root systems produced in soil by the forb and the grass, and the distinct root traits (e.g. root diameter and root tissue density) of the early- and late-successional plant species can explain the differences in the establishment of seedlings of plant species belonging to different groups of tropical succession when exposed to below-ground competition.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

AIDAR, M. P. M., SCHMIDT, S., MOSS, G., STEWART, G. R. & JOLY, C. A. 2003. Nitrogen use strategies of neotropical rainforest trees in threatened Atlantic Forest. Plant, Cell and Environment 26:389399.CrossRefGoogle Scholar
BALANDIER, P., COLLET, C., MILLER, J. H., REYNOLDS, P. E. & ZEDAKER, S. M. 2006. Designing forest vegetation management strategies based on the mechanisms and dynamics of crop tree competition by neighbouring vegetation. Forestry 70:327.Google Scholar
BRISSON, J. & REYNOLDS, J. F. 1994. The effect of neighbors on root distribution in a creosotebush (Larrea tridentata) population. Ecology 75:16931702.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
CAHILL, J. R. 2002. Interactions between root and shoot competition vary among species. Oikos 99:101112.Google Scholar
CLARK, L. J., WHALLEY, W. R. & BARRACLOUGH, P. B. 2003. How do roots penetrate strong soil? Plant and Soil 255:93104.CrossRefGoogle Scholar
CLARK, L. J., PRINCE, A. H., STEELE, K. A. & WHALLEY, W. R. 2008. Evidence for near-isogenic line that root penetration increases with root diameter and bending stiffness in rice. Functional Plant Biology 35:11631171.Google Scholar
CRAMER, M. D., WAKELING, J. L. & BOND, W. J. 2012. Belowground competitive suppression of seedling growth by grass in an African savanna. Plant Ecology 213:16551666.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 132:3443.Google Scholar
FAO. 1994. Soil map of the world. FAO-UNESCO, Rome. 140 pp.Google Scholar
FLORY, S. L. & CLAY, C. 2010. Non-native grass invasion suppresses forest succession. Oecologia 164:10291038.Google Scholar
GUNARATNE, A. M. T. A., GUNATILLEKE, C. V. S., GUNATILLEKE, I. A. U. N., MADAWALA WEERASINGHE, H. M. S. P. & BURSLEM, D. F. R. P. 2010. Barriers to tree seedling emergence on human-induced grasslands in Sri Lanka. Journal of Applied Ecology 47:157165.Google Scholar
GUNARATNE, A. M. T. A., GUNATILLEKE, C. V. S., GUNATILLEKE, I. A. U. N., MADAWALA WEERASINGHE, H. M. S. P. & BURSLEM, D. F. R. P. 2011. Release from root competition promotes tree seedling survival and growth following transplantation into human-induced grasslands in Sri Lanka. Forest Ecology and Management 262:229236.Google Scholar
HOLL, K. D. 1999. Factors limiting tropical rain forest regeneration in abandoned pasture: seed rain, seed germination, microclimate, and soil. Biotropica 31:229242.CrossRefGoogle Scholar
HOLL, K. D., LOIK, M. E., LIN, E. H. V. & SAMUELS, I. A. 2000. Tropical montane forest restoration in Costa Rica: overcoming barriers to dispersal and establishment. Restoration Ecology 8:339349.Google Scholar
HOOPER, E., CONDIT, R. & LEGENDRE, P. 2002. Responses of 20 native tree species to reforestation strategies for abandoned farmland in Panama. Ecological Application 12:16261641.Google Scholar
HOOPER, E., LEGENDRE, P. & CONDIT, R. 2005. Barriers to forest regeneration of deforested and abandoned land in Panama. Journal of Applied Ecology 42:11651174.Google Scholar
JOHNSON, N. C., NGELARD, C., SANDERS, I. R. & KIERS, E. T. 2013. Predicting community and ecosystem outcomes of mycorrhizal responses to global change. Ecological Letters 16:140153.Google Scholar
KEENEY, D. R. & NELSON, D. W. 1982. Nitrogen inorganic forms. Pp. 643698 in Page, A. L., Miller, R. H. & Keeney, D. R. (eds.). Methods of soil analysis, part 2: Chemical and microbiological properties. American Society of Agronomy, Madison.Google Scholar
KIERS, E. T., DUHAMEL, M., BEESETTY, Y., MENSAH, J. A., FRANKEN, O., VERBRUGGEN, E., FELLBAUM, C. R., KOWALCHUK, G. A., HART, M. M., BAGO, A., PALMER, T. M., WEST, S. A., VANDERNKOORNHUYSE, P., JANSA, J. & BÜCKING, H. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880882.Google Scholar
MATERECHERA, S. A., DEXTER, A. R. & ALSTON, A. M. 1991. Penetration of very strong soils by seedling roots of different plant species. Plant and Soil 135:3141.Google Scholar
MATERECHERA, S. A., ALSTON, A. M., KIRBY, J. M. & DEXTER, A. R. 1992. Influence of root diameter on the penetration of seminal roots into a compacted soil. Plant and Soil 144:297303.CrossRefGoogle Scholar
McCONNAUGHAY, K. D. M. C. & BAZZAZ, F. A. 1992. The occupation and fragmentation of space: consequences of neighboring roots. Functional Ecology 6:704710.Google Scholar
McGONIGLE, T. P., EVANS, D. G. & MILLER, M. H. 1990. Effects of degree of soil disturbance on mycorrhizal colonization and phosphorus absorption by maize in growth chamber and field experiments. New Phytologist 116:629636.Google Scholar
MESSIER, C., COLL, L., POITRAS-LARIVIÈRE, A., BÉLANGER, N. & BRISSON, J. 2009. Resource and non-resource root competition effects of grasses on early- versus late-successional trees. Journal of Ecology 97:548554.Google Scholar
NEPSTAD, D. C., UHL, C. & SERRAO, E. A. 1990. Surmounting barriers to forest regeneration in abandoned, highly degraded pastures: a case study from Paragominas, Pará, Brazil. Pp. 215229 in Anderson, A. (ed.). Alternatives to deforestation: steps towards sustainable uses of Amazonian forests. Columbia University Press, New York.Google Scholar
NEPSTAD, D. C., UHL, C., PEREIRA, C. A. & SILVA, J. M. C. 1996. A comparative study of tree establishment in abandoned pasture and mature forest of eastern Amazonia. Oikos 76:2539.Google Scholar
O'BRIEN, E. & BROWN, J. S. 2008. Games roots play; effects of soil volume and nutrients. Journal of Ecology 96:438446.Google Scholar
RILLIG, M. C. & MUMMEY, D. L. 2006. Mycorrhizas and soil structure. New Phytologist 171:4153.CrossRefGoogle ScholarPubMed
RONDINA, A. B. L., LESCANO, L. E. A. M., ALVES, R. A., MATSUURA, E. M., NOGUEIRA, M. A. & ZANGARO, W. 2014. Arbuscular mycorrhizas increase survival, precocity and flowering of herbaceous and shrubby species of early stages of tropical succession. Journal of Tropical Ecology 30:599614.Google Scholar
SELOSSE, M. & ROUSSET, F. 2011. The fungal-plant marketplace. Science 333:828829.Google Scholar
SUBBARAO, G. V., RONDON, M., ITO, O., ISHIKAWA, T., RAO, I. M., NAKAHARA, K., LASCANO, C. & BERRY, W. L. 2007. Biological nitrification inhibition (BNI) – is it a widespread phenomenon? Plant and Soil 294:518.CrossRefGoogle Scholar
SUBBARAO, G. V., NAKAHARA, K., HURTADO, M. P., ONO, H., MORETA, D. E., SALCEDO, A. F., YOSHIHASHI, A. T., ISHIKAWA, T., ISHITANIB, M., OHNISHI-KAMEYAMA, M., YOSHIDA, M., RONDON, M., RAO, I. M., LASCANO, C., BERRY, W. L. & ITO, O. 2009. Evidence for biological nitrification inhibition in Brachiaria pastures. Proceedings of National Academy of Sciences USA 106:1730217307.CrossRefGoogle ScholarPubMed
SUBBARAO, G. V., SAHRAWAT, K. L., NAKAHARA, K., RAO, I. M., ISHITANI, M., HASH, C. T., KISHII, M., BONNETT, D. G., BERRY, W. L. & LATA, J. C. 2012. A paradigm shift towards low-nitrifying production systems: the role of biological nitrification inhibition (BNI). Annals of Botany Special Issue:120.Google Scholar
TENNANT, D. 1975. A test modified line intersect method estimating root length. Journal of Ecology 63:9951001.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 16:603622.Google Scholar
ZANGARO, W., NISIZAKI, S. M. A., DOMINGOS, J. C. B. & NAKANO, E. M. 2003. Mycorrhizal response and successional status in 80 woody species from south Brazil. Journal of Tropical Ecology 19:315324.Google 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 21:529540.CrossRefGoogle Scholar
ZANGARO, W., NISHIDATE, F. R., VANDRESEN, J., ANDRADE, G. & NOGUEIRA, M. A. 2007. Root mycorrhizal colonization and plant responsiveness are related to root plasticity, soil fertility and succession status of native woody species in southern Brazil. Journal of Tropical Ecology 23:5362.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 roots traits in sites under different plant successional phases in southern Brazil. Mycorrhiza 19:3745.CrossRefGoogle ScholarPubMed
ZANGARO, W., ALVES, R. A., LESCANO, L. E. A. M., ANSANELO, A. P. & NOGUEIRA, M. A. 2012. Investment in fine roots and mycorrhizal fungi decrease during succession in three Brazilian ecosystems. Biotropica 44:141150.Google 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 23:221233.Google Scholar
ZANGARO, W., ALVES, R. A., SOUZA, P. B., ROSTIROLA, L. V., LESCANO, L. E. A. M., RONDINA, A. B. L. & NOGUEIRA, M. A. 2014. Succession and environmental variation influence soil exploration potential by fine roots and mycorrhizal fungi in an Atlantic ecosystem in southern Brazil. Journal of Tropical Ecology 30:237248.Google Scholar
ZANGARO, W., TOREZAN, J. M. D., ROSTIROLA, L. V., SOUZA, P. B. & NOGUEIRA, M. A. 2015. Influence of mycorrhizas, organic substrates and container volumes on the growth of Heliocarpus popayanensis Kunth. Cerne 21:395403.CrossRefGoogle Scholar