Transferência de nitrogênio entre plantas interconectadas por fungos micorrízicos arbusculares (FMAS)

Transfer of nitrogen between plants interconnected by arbuscular mycorrhizal fungi (AMF)

Resumos

Este trabalho, desenvolvido em casa de vegetação da Universidade Estadual do Norte Fluminense (UENF), em Campos (RJ), no primeiro semestre de 1996, objetivou avaliar a importância dos fungos micorrízicos arbusculares (FMAS) no processo de transferência de N do feijão para o milho, utilizando o isótopo 15N. Foram construídos três tipos de vasos especiais, divididos em três seções, A, B e C, com 2 dm³ de capacidade: sem barreira, com tela de nylon de 40 ∝m (permitiu a passagem de hifas fúngicas, mas não a de raízes) e com tela de nylon de 1 ∝m (não permitiu a passagem de hifas e raízes) entre as seções B e C. Adicionaram-se 25 mg kg-1 de N somente na seção A de cada vaso, utilizando-se, como fonte (15NH4)2SO4. Duas plantas de feijão pré-germinadas e inoculadas com Rhizobium tropici foram plantadas com suas raízes divididas entre as seções A e B. Após 10 dias, efetuou-se o plantio do milho, diretamente, na seção C dos vasos, e a inoculação micorrízica nos tratamentos com o FMA foi feita pela adição de propágulos de Glomus etunicatum somente na seção C. O experimento foi coletado 35 dias após o transplantio do feijão, e os resultados demonstraram que a colonização micorrízica se mostrou satisfatória, tanto no milho quanto no feijão. A presença da micorriza aumentou a produção de matéria seca, conteúdo de 15N e P da parte aérea das plantas de milho. A transferência direta de 15N do feijão para o milho através do micélio fúngico foi de 16,6%; a transferência indireta envolvendo o FMA - ou seja, a absorção do 15N excretado pelas raízes do feijão na solução do solo que foi absorvido e transferido através do micélio do FMA para o milho - foi de 34,1%; e a transferência indireta não envolvendo o FMA - ou seja, a absorção de 15N pelas raízes de milho da solução do solo sem envolvimento do FMA - foi de 49,3%.

micorriza; feijão; milho; nitrogênio


This work was undertaken at the State University of North Fluminense (UENF), State of Rio de Janeiro, Brazil, under greenhouse conditions, in the first semester of 1996, to evaluate the role of arbuscular mycorrhizal fungi (AMF) in the process of nitrogen transfer from bean to maize plants using the isotope 15N. Special pots divided in three sections (A, B and C), were constructed and either no barrier and a nylon mesh screen (40 ∝m) (which allowed the AMF hyphae to pass but not the plant roots) or 1 ∝m (which acted as barrier to AM hyphae and plant roots) was inserted between the sections B and C. It was added 25 mg kg-1 of N only into the section A, using as source (15NH4)2SO4. Two bean plants pre-germinated and inoculated with Rhizobium tropici were planted with their root systems divided between the sections A and B. Ten days later, 2 seeds of maize were sown into the section C and the inoculation was made by adding inoculum (Glomus etunicatum) into the substrate. Thirty-five days after the transplanting of the legume plants the experiment was harvested and the results revealed that the mycorrhizal colonization was satisfactory in maize and bean plants. The inoculation with AMF increased the dry weight and the 15N and P content of maize plant shoots. The direct transfer of 15N via AM hyphae was 16.6%; the indirect transfer of 15N mediated by AM mycelium network, was 34.1%, and the indirect transfer not mediated by AM mycelium network was 49.3%..

mycorrhizae; bean; maize; nitrogen


SEÇÃO III - BIOLOGIA DO SOLO

Transferência de nitrogênio entre plantas interconectadas por fungos micorrízicos arbusculares (FMAS)(1 (1 ) Parte da Dissertação de Mestrado do primeiro autor, apresentada à UENF, Campos (RJ). Trabalho financiado pela Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) e pelo Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). )

Transfer of nitrogen between plants interconnected by arbuscular mycorrhizal fungi (AMF)

A. F. CruzI; M. A. MartinsII

IEstudante de Mestrado da Universidade Estadual do Norte Fluminense (UENF), Av. Alberto Lamego, 2.000, CEP 28.015-620 Campos (RJ)

IIProfessor do Centro de Ciências e Tecnologias Agropecuárias da UENF, Setor de Microbiologia do Solo, Av. Alberto Lamego, 2.000, CEP 28.015-620 Campos (RJ). Bolsista do CNPq. E-mail: marco@uenf.br

RESUMO

Este trabalho, desenvolvido em casa de vegetação da Universidade Estadual do Norte Fluminense (UENF), em Campos (RJ), no primeiro semestre de 1996, objetivou avaliar a importância dos fungos micorrízicos arbusculares (FMAS) no processo de transferência de N do feijão para o milho, utilizando o isótopo 15N. Foram construídos três tipos de vasos especiais, divididos em três seções, A, B e C, com 2 dm3 de capacidade: sem barreira, com tela de nylon de 40 ∝m (permitiu a passagem de hifas fúngicas, mas não a de raízes) e com tela de nylon de 1 ∝m (não permitiu a passagem de hifas e raízes) entre as seções B e C. Adicionaram-se 25 mg kg-1 de N somente na seção A de cada vaso, utilizando-se, como fonte (15NH4)2SO4. Duas plantas de feijão pré-germinadas e inoculadas com Rhizobium tropici foram plantadas com suas raízes divididas entre as seções A e B. Após 10 dias, efetuou-se o plantio do milho, diretamente, na seção C dos vasos, e a inoculação micorrízica nos tratamentos com o FMA foi feita pela adição de propágulos de Glomus etunicatum somente na seção C. O experimento foi coletado 35 dias após o transplantio do feijão, e os resultados demonstraram que a colonização micorrízica se mostrou satisfatória, tanto no milho quanto no feijão. A presença da micorriza aumentou a produção de matéria seca, conteúdo de 15N e P da parte aérea das plantas de milho. A transferência direta de 15N do feijão para o milho através do micélio fúngico foi de 16,6%; a transferência indireta envolvendo o FMA - ou seja, a absorção do 15N excretado pelas raízes do feijão na solução do solo que foi absorvido e transferido através do micélio do FMA para o milho - foi de 34,1%; e a transferência indireta não envolvendo o FMA - ou seja, a absorção de 15N pelas raízes de milho da solução do solo sem envolvimento do FMA - foi de 49,3%.

Termos de indexação: micorriza, feijão, milho, nitrogênio.

SUMMARY

This work was undertaken at the State University of North Fluminense (UENF), State of Rio de Janeiro, Brazil, under greenhouse conditions, in the first semester of 1996, to evaluate the role of arbuscular mycorrhizal fungi (AMF) in the process of nitrogen transfer from bean to maize plants using the isotope 15N. Special pots divided in three sections (A, B and C), were constructed and either no barrier and a nylon mesh screen (40 ∝m) (which allowed the AMF hyphae to pass but not the plant roots) or 1 ∝m (which acted as barrier to AM hyphae and plant roots) was inserted between the sections B and C. It was added 25 mg kg-1 of N only into the section A, using as source (15NH4)2SO4. Two bean plants pre-germinated and inoculated with Rhizobium tropici were planted with their root systems divided between the sections A and B. Ten days later, 2 seeds of maize were sown into the section C and the inoculation was made by adding inoculum (Glomus etunicatum) into the substrate. Thirty-five days after the transplanting of the legume plants the experiment was harvested and the results revealed that the mycorrhizal colonization was satisfactory in maize and bean plants. The inoculation with AMF increased the dry weight and the 15N and P content of maize plant shoots. The direct transfer of 15N via AM hyphae was 16.6%; the indirect transfer of 15N mediated by AM mycelium network, was 34.1%, and the indirect transfer not mediated by AM mycelium network was 49.3%..

Index terms: mycorrhizae, bean, maize, nitrogen.

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AGRADECIMENTOS

Ao Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) e à FAPERJ, pelo apoio financeiro.

LITERATURA CITADA

AMES, R.N.; REID, C.P.P.; PARTER, L.K. & CAMBARDELLA, C. Sources by Glomus mosseae, a vesicular-arbuscular mycorrhizal fungus. New Phytol., Sheffield, 95:381-396, 1983.

BROPHY, L.S.; HEICHEL, G.H. & RUSSELLE, M.P. Nitrogen transfer from forage legumes to grass in a systematic planting design. Crop. Sci., Madison, 27:753-758, 1987.

BAREA, J.M.; AZCÓN-AGUILAR, C. & AZCÓN, R. Vesicular-Arbuscular mycorrhiza improve both symbiotic N2-fixation and N uptake from soil as assessed with a 15N technique under field conditions. New Phytol., Sheffield, 106:717-725. 1987.

BURTON, J.W.; BRIM, C.A. & RAWLINGS, J.O. Performance of non-nodulating and nodulating soybean isolines in mixed culture with nodulating cultivars. Crop Sci., Madison, 23:469-473, 1983.

CAMEL, S.B.; REYES-SOLIS, M.G.; FERRERA-CERRATO, R.; FRANSON, R.L.; BROWN, M.S. & BETHLENFALVAY, G.J. Growth of VA mycorrhizal mycelium through bulk soil. Soil Sci. Soc. Am. J., Madison, 55:389-393, 1991.

CATALDO, D.A.; SCHRADER, L.E. & YOUNGS, V.L. Analysis by digestion and colorimetric assay of total nitrogen in plant tissues high in nitrate. Crop. Sci., Madison, 14:854-856, 1974.

DUBACH, M. & RUSSELLE, M.P. Forage legumes roots and nodules and their role in the nitrogen transfer. Agron. J., Madison, 86:259-266, 1994.

FRANCIS, R. & READ, D.J. Direct transfer of carbon between plants connected by VA mycorrhizal mycelium. Nature, London, 307:53-56, 1984.

FRANCIS, R.; FINLAY, R.D. & READ, D.J. Transfer of nutrients in inter and intra-specific combination of host plants: Vesicular-Arbuscular mycorrhiza in natural vegetation systems. New Phytol., Sheffield, 102:103-111, 1986.

FREY, B. & SHUEPP, H. Transfer of symbiotically fixed nitrogen from berseen (Trifolium alexandrinum L.) to maize via VA mycorrhizal hyphae. New Phytol., Sheffield, 122:447-454, 1992.

GIOVANNETTI, M. & MOSSE, B. An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytol., Sheffield, 84:489-500, 1980.

HAMEL, C. & SMITH, D.L. Interspecific N-transfer and plant development in a mycorrhizal field-grown mixture. Soil Biol. Biochem., Oxford, 23:661-665, 1991.

HAMEL, C. & SMITH, D.L. Mycorrhizae-mediated 15N transfer from soybean to corn in field-grown intercrops. Effect of component crop spatial relationships. Soil Biol. Biochem., Oxford, 24:499-501, 1992.

HAYNES, R.J. Competitive aspects of the grass-legume association. Adv. Agron., New York, 33:227-261, 1980.

HAYSTEAD, A.; MALAJCZUK, N. & GROVE, T.S. Underground transfer of nitrogen between pasture plants infected with VA mycorrhizal fungi. New Phytol., Sheffield, 108:417-423, 1988.

IKRAM, A.; JENSEN, E.S. & JAKOBSEN, I. No significant transfer of N and P from Pueraria phaseoloides to Hevea brasiliensis via hyphal links of arbuscular mycorrhiza. Soil Biol. Biochem., Oxford, 26:1541-1547, 1994.

JOHANSEN, A. & JENSEN, E.S. Transfer of N and P from intact or decompositing roots of pea to barley interconnected by an arbuscular mycorrhizal fungus. Soil Biol. Biochem., Oxford, 28:73-81, 1996.

JOHANSEN, A.; JAKOBSEN, I. & JENSEN, E.S. Hyphal N transport by a vesicular-arbuscular mycorrhizal fungus associated with cucumber grown at 3 nitrogen levels. Plant Soil, The Hague, 160:1-9, 1994.

KESSEL, C.V.; SINGLETON, P.W. & HOBEN, H.J. Enhaced N-transfer from a soybean to maize. Plant Physiol., Bethesda, 79:562-563, 1985.

LEDGARD, S.F. Transfer of fixed nitrogen from white clover to associated grasses in swards grazed by dairy cows, estimated using 15N methods. Plant Soil, The Hague, 131:215-223, 1991.

MARTINS, M.A. The role of the external mycelial network of VA mycorrhizal fungi. A study of carbon transfer between plants interconnected by a common mycelium. Mycorrhiza, Berlin, 2:69-73, 1992a.

MARTINS, M.A. Interactions between plants with special reference to the role of the external mycelium of VA mycorrhizal fungi. Sheffield, The University of Sheffield, England, 1992b. 171p. (Tese de Doutorado)

MARTINS, M.A. The role of the external mycelial network of arbuscular mycorrhizal fungi in the carbon transfer process between plants. Mycol. Res., Cambridge, 97:807-810, 1993.

MARTINS, M.A. & READ, D.J. The role of the external mycelial network of VA mycorrhizal fungi. II. A study of phosphorus transfer between plants interconnected by a common mycelium. R. Microb., São Paulo, 27: 30-35, 1996.

MOSSE, B. Specificity in VA mycorrhizas. In: SANDERS, F.E.; MOSSE, B. & TINKER, P.B., eds. Endomycorrhizas. London, Academic Press, 1975. p. 469-484.

NEWMAN, E.I. Mycorrhizal links between plants: their functioning and ecological significance. Adv. Ecol. Res., London, 18:243-270. 1988.

NEWMAN, E.I. & RITZ, K. Evidence on the pathway of phosphorus transfer between VA mycorrhizal plants. New Phytol., Sheffield, 104:77-87, 1986.

NEWMAN, E.I. & EASON, W.R. Rates of phosphorus transfer within and between ryegrass (Lolium perenne) plants.Funct. Ecol., Sheffield, 7:242-248, 1993.

POWELL, C.L. Development of mycorhizal infection from endogone spores infected root segments. Trans Br. Mycol. Soc., London, 66:439-445, 1976.

RAO, A.V. & GILLER, K.E. Nitrogen fixation and its transfer from Leucaena to Grass using N15. Ecol. Manag., 61:221-227, 1994.

READ, D.J. The structure and function of the vegetative mycelium of mycorrhizal roots. In: JENNINGS, D.H. & RAYNER, A.D.M. eds. The ecology and physiology of the fungal mycelium. Cambridge, Cambridge University Press, 1984. p.215-240.

READ, D.J. & BIRCH, C.P.D. The effects and implications of disturbance of mycorrhizal mycelial systems. Proc. Royal Soc. Edinb., Edingburg, 94:13-24, 1986.

READ, D.J.; KOUCHECKI, H.K. & HODGSON, J. VA mycorrhiza in natural vegetation systems. I. The occurrence of infection. New Phytol., Sheffield, 77:641-653, 1976.

REDMON, L.A.; ROUQUETE, F.M.; SMITH Jr., G.R. & STUTH, J.W. Nitrogen transfer from warm-season annual legumes to pearl millet. J. Plant Nut., New York, 18:803-813, 1995.

RITZ, K. & NEWMAN, E.I. Evidence for rapid cycling of phosphorus from dying roots to living plants. Oikos, Copenhagen, 45:174-180, 1985.

TOMM, G.O.; KESSEL, G.V. & SLINKARD, A.E. Bidirectional transfer of nitrogen between alfafa and bromegrass: Short and long term evidence. Plant Soil, The Hague, 164:77-86, 1994.

TOMMERUP, I.C. Spore dormancy in VA mycorrhizal fungi. Trans. Br. Mycol. Soc., Cambridge, 81:37-45, 1983.

TOMMERUP, I.C. & ABBOTT, L.K. Prolonged survival and viability of VA mycorrhizal hyphae after root death. Soil Biol. Biochem., Oxford, 13:431-433, 1981.

VAN KESSEL, C.; SINGLETON, P.W. & HOBEN, H. Enhanced N-transfer from a soybean to maize by VA mycorrhizal fungi. Plant Physiol., Bethesda, 79:562-563, 1985.

Recebido para publicação em outubro de 1996

Aprovado em julho de 1997

  • AMES, R.N.; REID, C.P.P.; PARTER, L.K. & CAMBARDELLA, C. Sources by Glomus mosseae, a vesicular-arbuscular mycorrhizal fungus. New Phytol., Sheffield, 95:381-396, 1983.
  • BROPHY, L.S.; HEICHEL, G.H. & RUSSELLE, M.P. Nitrogen transfer from forage legumes to grass in a systematic planting design. Crop. Sci., Madison, 27:753-758, 1987.
  • BAREA, J.M.; AZCÓN-AGUILAR, C. & AZCÓN, R. Vesicular-Arbuscular mycorrhiza improve both symbiotic N2-fixation and N uptake from soil as assessed with a 15N technique under field conditions. New Phytol., Sheffield, 106:717-725. 1987.
  • BURTON, J.W.; BRIM, C.A. & RAWLINGS, J.O. Performance of non-nodulating and nodulating soybean isolines in mixed culture with nodulating cultivars. Crop Sci., Madison, 23:469-473, 1983.
  • CAMEL, S.B.; REYES-SOLIS, M.G.; FERRERA-CERRATO, R.; FRANSON, R.L.; BROWN, M.S. & BETHLENFALVAY, G.J. Growth of VA mycorrhizal mycelium through bulk soil. Soil Sci. Soc. Am. J., Madison, 55:389-393, 1991.
  • CATALDO, D.A.; SCHRADER, L.E. & YOUNGS, V.L. Analysis by digestion and colorimetric assay of total nitrogen in plant tissues high in nitrate. Crop. Sci., Madison, 14:854-856, 1974.
  • DUBACH, M. & RUSSELLE, M.P. Forage legumes roots and nodules and their role in the nitrogen transfer. Agron. J., Madison, 86:259-266, 1994.
  • FRANCIS, R. & READ, D.J. Direct transfer of carbon between plants connected by VA mycorrhizal mycelium. Nature, London, 307:53-56, 1984.
  • FRANCIS, R.; FINLAY, R.D. & READ, D.J. Transfer of nutrients in inter and intra-specific combination of host plants: Vesicular-Arbuscular mycorrhiza in natural vegetation systems. New Phytol., Sheffield, 102:103-111, 1986.
  • FREY, B. & SHUEPP, H. Transfer of symbiotically fixed nitrogen from berseen (Trifolium alexandrinum L.) to maize via VA mycorrhizal hyphae. New Phytol., Sheffield, 122:447-454, 1992.
  • GIOVANNETTI, M. & MOSSE, B. An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytol., Sheffield, 84:489-500, 1980.
  • HAMEL, C. & SMITH, D.L. Interspecific N-transfer and plant development in a mycorrhizal field-grown mixture. Soil Biol. Biochem., Oxford, 23:661-665, 1991.
  • HAMEL, C. & SMITH, D.L. Mycorrhizae-mediated 15N transfer from soybean to corn in field-grown intercrops. Effect of component crop spatial relationships. Soil Biol. Biochem., Oxford, 24:499-501, 1992.
  • HAYNES, R.J. Competitive aspects of the grass-legume association. Adv. Agron., New York, 33:227-261, 1980.
  • HAYSTEAD, A.; MALAJCZUK, N. & GROVE, T.S. Underground transfer of nitrogen between pasture plants infected with VA mycorrhizal fungi. New Phytol., Sheffield, 108:417-423, 1988.
  • IKRAM, A.; JENSEN, E.S. & JAKOBSEN, I. No significant transfer of N and P from Pueraria phaseoloides to Hevea brasiliensis via hyphal links of arbuscular mycorrhiza. Soil Biol. Biochem., Oxford, 26:1541-1547, 1994.
  • JOHANSEN, A. & JENSEN, E.S. Transfer of N and P from intact or decompositing roots of pea to barley interconnected by an arbuscular mycorrhizal fungus. Soil Biol. Biochem., Oxford, 28:73-81, 1996.
  • JOHANSEN, A.; JAKOBSEN, I. & JENSEN, E.S. Hyphal N transport by a vesicular-arbuscular mycorrhizal fungus associated with cucumber grown at 3 nitrogen levels. Plant Soil, The Hague, 160:1-9, 1994.
  • KESSEL, C.V.; SINGLETON, P.W. & HOBEN, H.J. Enhaced N-transfer from a soybean to maize. Plant Physiol., Bethesda, 79:562-563, 1985.
  • LEDGARD, S.F. Transfer of fixed nitrogen from white clover to associated grasses in swards grazed by dairy cows, estimated using 15N methods. Plant Soil, The Hague, 131:215-223, 1991.
  • MARTINS, M.A. The role of the external mycelial network of VA mycorrhizal fungi. A study of carbon transfer between plants interconnected by a common mycelium. Mycorrhiza, Berlin, 2:69-73, 1992a.
  • MARTINS, M.A. Interactions between plants with special reference to the role of the external mycelium of VA mycorrhizal fungi. Sheffield, The University of Sheffield, England, 1992b. 171p. (Tese de Doutorado)
  • MARTINS, M.A. The role of the external mycelial network of arbuscular mycorrhizal fungi in the carbon transfer process between plants. Mycol. Res., Cambridge, 97:807-810, 1993.
  • MARTINS, M.A. & READ, D.J. The role of the external mycelial network of VA mycorrhizal fungi. II. A study of phosphorus transfer between plants interconnected by a common mycelium. R. Microb., São Paulo, 27: 30-35, 1996.
  • MOSSE, B. Specificity in VA mycorrhizas. In: SANDERS, F.E.; MOSSE, B. & TINKER, P.B., eds. Endomycorrhizas. London, Academic Press, 1975. p. 469-484.
  • NEWMAN, E.I. Mycorrhizal links between plants: their functioning and ecological significance. Adv. Ecol. Res., London, 18:243-270. 1988.
  • NEWMAN, E.I. & RITZ, K. Evidence on the pathway of phosphorus transfer between VA mycorrhizal plants. New Phytol., Sheffield, 104:77-87, 1986.
  • NEWMAN, E.I. & EASON, W.R. Rates of phosphorus transfer within and between ryegrass (Lolium perenne) plants.Funct. Ecol., Sheffield, 7:242-248, 1993.
  • POWELL, C.L. Development of mycorhizal infection from endogone spores infected root segments. Trans Br. Mycol. Soc., London, 66:439-445, 1976.
  • RAO, A.V. & GILLER, K.E. Nitrogen fixation and its transfer from Leucaena to Grass using N15 Ecol. Manag., 61:221-227, 1994.
  • READ, D.J. The structure and function of the vegetative mycelium of mycorrhizal roots. In: JENNINGS, D.H. & RAYNER, A.D.M. eds. The ecology and physiology of the fungal mycelium. Cambridge, Cambridge University Press, 1984. p.215-240.
  • READ, D.J. & BIRCH, C.P.D. The effects and implications of disturbance of mycorrhizal mycelial systems. Proc. Royal Soc. Edinb., Edingburg, 94:13-24, 1986.
  • READ, D.J.; KOUCHECKI, H.K. & HODGSON, J. VA mycorrhiza in natural vegetation systems. I. The occurrence of infection. New Phytol., Sheffield, 77:641-653, 1976.
  • REDMON, L.A.; ROUQUETE, F.M.; SMITH Jr., G.R. & STUTH, J.W. Nitrogen transfer from warm-season annual legumes to pearl millet. J. Plant Nut., New York, 18:803-813, 1995.
  • RITZ, K. & NEWMAN, E.I. Evidence for rapid cycling of phosphorus from dying roots to living plants. Oikos, Copenhagen, 45:174-180, 1985.
  • TOMM, G.O.; KESSEL, G.V. & SLINKARD, A.E. Bidirectional transfer of nitrogen between alfafa and bromegrass: Short and long term evidence. Plant Soil, The Hague, 164:77-86, 1994.
  • TOMMERUP, I.C. Spore dormancy in VA mycorrhizal fungi. Trans. Br. Mycol. Soc., Cambridge, 81:37-45, 1983.
  • TOMMERUP, I.C. & ABBOTT, L.K. Prolonged survival and viability of VA mycorrhizal hyphae after root death. Soil Biol. Biochem., Oxford, 13:431-433, 1981.
  • VAN KESSEL, C.; SINGLETON, P.W. & HOBEN, H. Enhanced N-transfer from a soybean to maize by VA mycorrhizal fungi. Plant Physiol., Bethesda, 79:562-563, 1985.

  • (1
    ) Parte da Dissertação de Mestrado do primeiro autor, apresentada à UENF, Campos (RJ). Trabalho financiado pela Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) e pelo Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

Datas de Publicação

  • Publicação nesta coleção
    08 Out 2014
  • Data do Fascículo
    Dez 1997

Histórico

  • Recebido
    Out 1996
  • Aceito
    Jul 1997
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