Growth Traits and the Trade-Offs for Tree Species with Arbuscular Mycorrhizal Fungi in a Tropical Rain Forest Edge at Los Tuxtlas, Mexico

Abstract

The effect of arbuscular mycorrhizal fungi on seedling growth across the rain forest-pasture edge has not received much attention. In a tropical rain forest in eastern Mexico, the seedlings of light demanding (Ficus insipida), nonsecondary light demanding (Lonchocarpus cruentus) and shade tolerant species (Nectandra ambigens, Coccoloba hondurensis) were grown and transplanted to a forest edge with three inoculation treatments (AM fungus spores and colonized roots, spores, and no inoculum). For all species, stem height, stem diameter, total dry weight, leaf area and net assimilation rate were higher in the pasture. Stem height, stem diameter and root/shoot were higher for L. cruentus, and leaf area ratio, specific leaf area and net assimilation rate were higher for F. insipida; the lowest values of almost all variables were recorded for N. ambigens. L. cruentus and C. hondurensis with mycorrhizae had the highest values for root/shoot and net assimilation rate, respectively. The lowest values of root/shoot and net assimilation rate were observed for nonlight-demanding species in the forest. There were clear trade-offs for the pioneer species between survival and growth, and in underground biomass allocation and assimilation for nonsecondary light demanding, but there was not for the shade-tolerant species.

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Peña-Becerril, J. , Álvarez-Sánchez, J. , Barajas-Guzmán, G. and Quiroz-Ayala, A. (2015) Growth Traits and the Trade-Offs for Tree Species with Arbuscular Mycorrhizal Fungi in a Tropical Rain Forest Edge at Los Tuxtlas, Mexico. Open Journal of Forestry, 5, 181-194. doi: 10.4236/ojf.2015.52017.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Achard, F., Eva, H. D., Stibig, H.-J., Mayaux, P., Gallego, J., Richards, T., & Malingreau, J. P. (2002). Determination of Deforestation Rates of the World’s Humid Tropical Forests. Science, 297, 999-1002.
http://dx.doi.org/10.1126/science.1070656
[2] Ackerly, D. D., Knight, C. A., Weiss, S. B., & Barton, K. (2002). Leaf Size, Specific Leaf Area and Microhabitat Distribution of Chaparral Woody Plants: Contrasting Patterns in Species Level and Community Level Analyses. Oecologia, 130, 449-457.
http://dx.doi.org/10.1007/s004420100805
[3] Allen, E. B., Allen, M. F., Egerton-Warburton, L., Corkidi, L., & Gómez-Pompa, A. (2003). Impacts of Early- and Late-Seral Mycorrhizae during Restoration in Seasonal Tropical Forest, Mexico. Ecological Applications, 13, 1701-1717.
http://dx.doi.org/10.1890/02-5309
[4] Allen, M. F. (1991). The Ecology of Mycorrhizae. Cambridge: Cambridge University Press.
[5] álvarez-Sánchez, J., Guadarrama, P., Sánchez-Gallen, I., & Olivera, D. (2007). Restauración de ambientes deteriorados derivados de la selva húmeda: El uso de los hongos micorrizógenos arbusculares. Boletín de la Sociedad Botánica de México, 80, 59-68.
[6] álvarez-Sánchez, J., Sánchez-Gallen, I., & Guadarrama, P. (2009). Ch. 18: Analysis of Ecophysiological Traits of Tropical rain Forest Seedlings under Arbuscular Mycorrhization: Implications in Ecological Restoration. In A. Varma, & A. C. Kharkwal (Eds.), Symbiotic Fungi: Principles and Practice (pp. 293-305). Berlin: Springer-Verlag.
http://dx.doi.org/10.1007/978-3-540-95894-9_18
[7] Arroyo-Rodríguez, V., & Mandujano, S. (2007). Ch. 7: Efectos de la fragmentación sobre la composición y la estructura de un bosque tropical lluvioso mexicano. In C. A. Harvey, & J. C. Sáenz (Eds.), Evaluación y conservación de biodiversidad en paisajes fragmentados de Mesoamérica (pp. 179-196). Costa Rica: Instituto Nacional de Biodiversidad (INBio).
[8] Arroyo-Rodríguez, V., Dunn, J. C., Benítez-Malvido, J., & Mandujano, S. (2009). Angiosperms, Los Tuxtlas Biosphere Reserve, Veracruz, Mexico. Check List, Journal of Species Lists and Distribution, 5, 787-799. http://www.checklist.org.br
[9] Benítez-Malvido, J., & Martínez-Ramos, M. (2003). Influence of Edge Exposure on Tree Seedling Species Recruitment in Tropical Rain Forest Fragments. Biotropica, 35, 530-541.
http://dx.doi.org/10.1111/j.1744-7429.2003.tb00609.x
[10] Cai, Z. Q., Poorter, L., Han, Q., & Bongers, F. (2008). Effects of Light and Nutrients on Seedlings of Tropical Bauhinia Lianas and Trees. Tree Physiology, 28, 1277-1285.
http://dx.doi.org/10.1093/treephys/28.8.1277
[11] Castillo-Campos, G., & Laborde, J. (2004). Ch. 12: La vegetación. In S. Guevara, J. Laborde, & G. Sánchez-Ríos (Eds.), Los Tuxtlas, el paisaje de la sierra (pp. 41-55). Xalapa: Instituto de Ecología, A.C.
[12] Cuenca, G., Lovera, M., Fajardo, L., & Meneses, E. (2006). Efecto de las micorrizas arbusculares sobre el crecimiento y supervivencia de dos especies nativas de la gran sabana, al transplantarlas a un área degradada. Acta Científica Venezolana, 57, 42-48.
[13] Dalling, J. W., & Hubbell, S. P. (2002). Seed Size, Growth Rate and Gap Microsite Conditions as Determinants of Recruitment Success for Pioneer Species. Journal of Ecology, 90, 557-568.
http://dx.doi.org/10.1046/j.1365-2745.2002.00695.x
[14] Daniels, B., & Skipper, H. (1982). Methods for the Recovery and Quantitative Estimation of Propagules from Soil. In N. Schenck (Ed.), Methods and Principles of Mycorrhiza Research (pp. 29-37). Minnesota: American Society for Phytopathology.
[15] Davies, S. J. (2001). Tree Mortality and Growth in 11 Sympatric Macaranga Species in Borneo. Ecology, 82, 920-932.
http://dx.doi.org/10.1890/0012-9658(2001)082[0920:TMAGIS]2.0.CO;2
[16] Escamilla, H. N. (2009). Características del suelo en un borde selva-potrero en los Tuxtlas, Veracruz. Bachelor Thesis, México City: Universidad Nacional Autónoma de México.
[17] Flores-Delgadillo, L., Sommer-Cervantes, I., Alcalá-Martínez, J. R., & álvarez-Sánchez, J. (1999). Estudio morfogenético de algunos suelos de la región de los Tuxtlas, Veracruz, México. Revista Mexicana de Ciencias Geológicas, 16, 81-88.
[18] Gehring, C. A. (2003). Growth Responses to Arbuscular Mycorrhizae by Rain Forest Seedlings Vary with Light Intensity and Tree Species. Plant Ecology, 167, 127-139.
http://dx.doi.org/10.1023/A:1023989610773
[19] Gehring, C. A., & Connell, J. H. (2006). Arbuscular Mycorrhizal Fungi in the Tree Seedlings of Two Australian Rain Forests: Occurrence, Colonization, and Relationships with Plant Performance. Mycorrhiza, 16, 89-98.
http://dx.doi.org/10.1007/s00572-005-0018-5
[20] Gerdemann, J. W., & Nicolson, T. H. (1963). Spores of Mycorrhizal Endogone Species Extracted from Soil by Wet Sieving and Decanting. Transactions of the British Mycological Society, 46, 235-244.
http://dx.doi.org/10.1016/S0007-1536(63)80079-0
[21] Guadarrama, P., álvarez-Sánchez, J., & Briones, O. (2004). Seedling Growth of Two Pioneer Tropical Tree Species in Competition: The Role of Arbuscular Mycorrhizae. Euphytica, 138, 113-121.
http://dx.doi.org/10.1023/B:EUPH.0000046797.42632.6b
[22] Guariguata, M., & Ostertag, R. (2001). Neotropical Secondary Forest Succssesion: Changes in Structural and Functional Characteristics. Forest Ecology and Management, 148, 185-206.
http://dx.doi.org/10.1016/S0378-1127(00)00535-1
[23] Guevara, S., Laborde, J., & Sánchez-Ríos, G. (2004a). Ch. 5: La fragmentación. In S. Guevara, J. Laborde, & G. Sánchez-Ríos (Eds.), Los Tuxtlas, el paisaje de la sierra (pp. 111-134). Xalapa: Instituto de Ecología, A.C.
[24] Guevara, S., Laborde, J., & Sánchez-Ríos, G. (2004b). Rain Forest Regeneration beneath the Canopy of Fig Trees Isolated in Pastures of Los Tuxtlas, Mexico. Biotropica, 36, 99-108.
[25] Harper, K. A., Macdonald, A. E., Burton, P. J., Jiquan, C., Brosofske, K. D., Saunders, S. C. et al. (2005). Edge Influence on Forest Structure and Composition in Fragmented Landscapes. Conservation Biology, 19, 768-782.
http://dx.doi.org/10.1111/j.1523-1739.2005.00045.x
[26] Hunt, R. (1982). Plant Growth Analysis. London: Natural Environment Research Council.
[27] Jeffries, P., Gianinazzi, S., Perotto, S., Turnau, K., & Barea, J. M. (2003). The Contribution of Arbuscular Mycorrhizal Fungi in Sustainable Maintenance of Plant Health and Soil Fertility. Biology and Fertility of Soils, 37, 1-16.
[28] Kitajima, K, & Fenner, M. (2000). Ecology of Seedling Regeneration. In M. Fenner (Ed.), Seeds: The Ecology of Regeneration in Plant Communities (pp. 331-359). London: CAB Publishing.
http://dx.doi.org/10.1079/9780851994321.0331
[29] Kitajima, K. (1994). Relative Importance of Photosynthetic Traits and Allocation Patterns as Correlates of Seedling Shade Tolerance of 13 Tropical Trees. Oecologia, 98, 419-428. http://dx.doi.org/10.1007/BF00324232
[30] Koele, N., Dickie, I. A., Oleksyn, J., Richardson, S. J., & Reich, P. B. (2012). No Globally Consistent Effect of Ectomycorrhizal Status on Foliar Traits. New Phytologist, 196, 845-852.
http://dx.doi.org/10.1111/j.1469-8137.2012.04297.x
[31] Lambers, H., & Poorter, H. (1992). Inherent Variation in Growth Rate between Higher Plants: A Search for Physiological Causes and Ecological Consequences. Advances in Ecological Research, 23, 188-261.
http://dx.doi.org/10.1016/S0065-2504(08)60148-8
[32] Laurance, W. F. (2004). Forest-Climate Interactions in Fragmented Tropical Landscapes. Philosophical Transactions: Biological Sciences, 359, 345-352.
http://dx.doi.org/10.1098/rstb.2003.1430
[33] Lovelock, C. E., Andersen, K., & Morton, J. B. (2003). Arbuscular Mycorrhizal Communities in Tropical Forest Are Affected by Host Tree Species and Environment. Oecologia, 135, 268-279.
[34] Martínez-Garza, C., Pena, V., Ricker, M., Campos, A., & Howe, H. F. (2005). Restoring Tropical Biodiversity: Leaf Traits Predict Growth and Survivorship of Late-Successional Trees in Early-Successional Environments. Forest Ecology and Management, 217, 365-379.
http://dx.doi.org/10.1016/j.foreco.2005.07.001
[35] Montgomery, R. A., & Chazdon, R. L. (2002). Light Gradient Partitioning by Tropical Tree Seedlings in the Absence of Canopy Gaps. Oecologia, 131, 165-174.
http://dx.doi.org/10.1007/s00442-002-0872-1
[36] Oehl, F., Sieverding, E., Ineichen, K., Mader, P., Boller, T., & Wiemken, A. (2003). Impact of Land Use Intensity on the Species Diversity of Arbuscular Mycorrhizal Fungi in Agroecosystems of Central Europe. Applied and Environmental Microbiology, 69, 2816-2824.
http://dx.doi.org/10.1128/AEM.69.5.2816-2824.2003
[37] Parolin, P., Ferreira, L. V., & Junk, W. J. (2003). Germination Characteristics and Establishment of Trees from Central Amazonian Flood Plains. Tropical Ecology, 44, 157-169.
[38] Phillips, J. M., & Hayman, D. S. (1970). Improved Procedures for Clearing Roots and Staining Parasitic and Vesicualr-Arbuscular Mycorrhizal Fungi for Rapid Assessment of Infection. Transactions of the British Mycological Society, 55, 158-161.
http://dx.doi.org/10.1016/S0007-1536(70)80110-3
[39] Picone, C. (2000). Diversity and Abundance of Arbuscular-Mycorrhizal Fungus Spores in Tropical Forest and Pasture. Biotropica, 32, 734-750.
http://dx.doi.org/10.1646/0006-3606(2000)032[0734:DAAOAM]2.0.CO;2
[40] Plenchette, C., Fortin, J. A., & Furlan, V. (1983). Growth Response of Several Plants Species to Mycorrhiza in a Soil of Moderate P-Fertility. Plant and Soil, 70, 191-209.
http://dx.doi.org/10.1007/BF02374781
[41] Pohlman, C. L., Turton, S. M., & Goosem, M. (2007). Edge Effects of Linear Canopy Openings on Tropical Rain Forest Understory Microclimate. Biotropica, 39, 62-71.
http://dx.doi.org/10.1111/j.1744-7429.2006.00238.x
[42] Poorter, H., & Van Der Werf, A. (1998). Is Inherent Variation in RGR Determined by LAR at Low Irradiance and by NAR at High Irradiance? A Review of Herbaceous Species. In H. Lambers, H. Poorter, M. M. I., & M. Van Vuuren (Eds.), Inherent Variation in Plant Growth. Physiological Mechanisms and Ecological Consequences (pp. 309-336). Leiden, AH: Backhuys Publishers.
[43] Pouyú-Rojas, E., & Siqueira, J. O. (2000). Micorriza arbuscular e fertilizacao do solo no desenvolvimento pós-transplante de mudas de sete espécies florestais. Pesquisa Agropecuária Brasileira, 35, 103-114.
http://dx.doi.org/10.1590/S0100-204X2000000100013
[44] Reich, P. B., Walters, M. B., & Ellsworth, D. S. (1997). From Tropics to Tundra: Global Convergence in Plant Functioning. Proceedings of the National Academy of Sciences of the United States of America, 94, 13730-13734.
http://dx.doi.org/10.1073/pnas.94.25.13730
[45] Reich, P. B., Wright, I. J., Cavender-Bares, J., Craine, J. M., Oleksyn, J., Westoby, M., & Walters, M. B. (2003). The Evolution of Plant Functional Variation: Traits, Spectra, and Strategies. International Journal of Plant Sciences, 164, 143-164.
http://dx.doi.org/10.1086/374368
[46] Rilling, M. C. (2004). Arbuscular Mycorrhizae and Terrestrial Ecosystem Processes. Ecology Letters, 7, 740-754.
http://dx.doi.org/10.1111/j.1461-0248.2004.00620.x
[47] Rincón, E., & Huante, P. (1993). Growth Responses of Tropical Deciduous Tree Seedlings to Contrasting Light Conditions. Trees, 7, 202-207.
http://dx.doi.org/10.1007/BF00202074
[48] Rodríguez, J. (2006). Efectos de la defoliación inducida sobre el crecimiento de tres arbustos riberenos de la Sierra tarahumara bajo condiciones de crecimiento en rizotrón. Master Thesis, México City: Universidad Nacional Autónoma de México.
[49] Rozendaal, D. M. A., Hurtado, V. H., & Poorter, L. (2006). Plasticity in Leaf Traits of 38 Tropical Tree Species in Response to Light: Relationships with Light Demand and Adult Stature. Functional Ecology, 20, 207-216.
http://dx.doi.org/10.1111/j.1365-2435.2006.01105.x
[50] Saldana-Acosta, A., Meave, J. A., Paz, H., Sánchez-Velásquez, L. R., Villasenor, J. L., & Martínez-Ramos, M. (2008). Variation of Functional Traits in Trees from a Biogeographically Complex Mexican Cloud Forest. Acta Oecologica, 34, 111-121.
http://dx.doi.org/10.1016/j.actao.2008.04.006
[51] Sánchez-Gallen, I. (2011). Análisis de la comunidad de plántulas, en relación con la de hongos micorrizógenos arbusculares, en fragmentos de vegetación remanente de una selva húmeda. Ph.D. Thesis, México City: Universidad Nacional Autónoma de México.
[52] Sanderss, I. R., Koide, R. T., & Shumway, D. L. (1995). Community-Level Interactions between Plants and Vesicular-Arbuscular Mycorrhizal Fungi. In A. Varma, & B. Hock (Eds.), Mycorrhiza: Structure, Function, Molecular Biology and Biotechnology (pp. 607-625). Berlin: Springer-Verlag.
http://dx.doi.org/10.1007/978-3-662-08897-5_26
[53] Selaya, N. G., Oomen, R. J., Netten, J. J. C., Werger, M. J. A., & Anten, N. P. R. (2008). Biomass Allocation and Leaf Life Span in Relation to Light Interception by Tropical Forest Plants during the First Years of Secondary Succession. Journal of Ecology, 96, 1211-1221.
http://dx.doi.org/10.1111/j.1365-2745.2008.01441.x
[54] Smith, S. E., & Read, D. J. (2008). Mycorrhizal Symbiosis. San Diego, CA: Academic Press.
[55] Sommer-Cervantes, I., Flores-Delgadillo, L., & Gutiérrez-Ruiz, M. (2003). Ch. 1: Caracterización de los suelos de la Estación de Biología Tropical Los Tuxtlas. In J. álvarez-Sánchez, & E. Naranjo-García (Eds.), Ecología del suelo en la selva tropical húmeda de México (pp. 17-67). Xalapa: Instituto de Ecología, A.C.
[56] Soto, M., & Gama, L. (1997). Ch. 2: Climas. In S. E. González, R. Dirzo, & R. C. Vogt (Eds.), Historia natural de Los Tuxtlas. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (pp. 7-23). México City: Instituto de Biología, Instituto de Ecología, UNAM.
[57] Strauss-Debenedetti, S., & Bazzaz, F. A. (1996). Photosynthetic Characteristics of Tropical Trees along Successional Gradients. In S. S. Mulkey, R. L. Chazdon, & A. P. Smith (Eds.), Tropical Forest Plant Ecophysiology (pp. 162-186). New York: Chapman & Hall Press.
http://dx.doi.org/10.1007/978-1-4613-1163-8_6
[58] Stürmer, S. L., & Siqueira, J. O. (2010). Species Richness and Spore Abundance of Arbuscular Mycorrhizal Fungi across Distinct Land Uses in Western Brazilian Amazon. Mycorrhiza, 21, 255-267.
http://dx.doi.org/10.1007/s00572-010-0330-6
[59] Tedersoo, L, Sadam, A., Zambrano, M., Valencia, R., & Bahram, M. (2010). Low Diversity and High Host Preference of Ectomycorrhizal Fungi in Western Amazonia, a Neotropical Biodiversity Hotspot. The ISME Journal, 4, 465-471.
http://dx.doi.org/10.1038/ismej.2009.131
[60] Turner, I. M. (2001). The Ecology of Trees in the Tropical Rain Forest. Cambridge: Cambridge University Press.
http://dx.doi.org/10.1017/CBO9780511542206
[61] Van der Heijden, M. G. A., Klironomos, J. N., Ursic, M., Moutoglis, P., Streitwolf-Engel, R., Boller, T. et al. (1998). Mycorrhizal Fungal Diversity Determines Plant Biodiversity, Ecosystem Variability and Productivity. Nature, 396, 69-72.
http://dx.doi.org/10.1038/23932
[62] Varela, L., Trejo, D., álvarez-Sánchez, J., Barois, I., Amora-Lazcano, E., Guadarrama, P. et al. (2009). Ch. 6: Land Use and Diversity of Arbuscular Mycorrhizal Fungi in Mexican Tropical Ecosystems: Preliminary Results. In I. Barois, E. J. Huising, P. Okoth, D. Trejo, & M. de los Santos (Eds.), Below-Ground Biodiversity in Sierra Santa Marta, Los Tuxtlas, Veracruz, Mexico (pp. 99-112). Xalapa: Instituto de Ecología, A.C.
[63] Violi, H. A., Barrientos-Priego, A. F., Wright, S. G., Escamilla-Prado, E., Morton, J. B., Menge, J. A., & Lovatt, C. J. (2008). Disturbance Changes Arbuscular Mycorrhizal Fungal Phenology and Soil Glomalin Concentrations but Not Fungal Spore Composition in Montane Rain Forest in Veracruz and Chiapas, Mexico. Forest Ecology and Management, 254, 276-290.
http://dx.doi.org/10.1016/j.foreco.2007.08.016
[64] Walters, M. B., & Reich, P. B. (1999). Low-Light Carbon Balance and Shade Tolerance in the Seedlings of Woody Plants: Do Winter Deciduous and Broad-Leaved Evergreen Species Differ? New Phytologist, 143, 143-154.
http://dx.doi.org/10.1046/j.1469-8137.1999.00425.x
[65] Wright, I. J., Reich, P. B., Cornelissen, J. H. C., Falster, D. S., Garnier, E., Hikosaka, K. et al. (2005). Assessing the Generality of Global Leaf Trait Relationships. New Phytologist, 166, 485-496.
http://dx.doi.org/10.1111/j.1469-8137.2005.01349.x
[66] Wright, J. S., Kitajima, K., Kraft, N. J. B., Reich, P. B., Wright, I. J., Bunker, D. E. et al. (2010). Functional Traits and the Growth-Mortality Trade-Off in Tropical Trees. Ecology, 91, 3364-3674.
http://dx.doi.org/10.1890/09-2335.1
[67] Zangaro, W., Bononi, V. L., & 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.
http://dx.doi.org/10.1017/S0266467400001607
[68] Zangaro, W., Nishidate, F. R., Camargo, F. R. S., Romagnoli, G. G., & Vandressen, 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.
http://dx.doi.org/10.1017/S0266467405002555
[69] Zangaro, W., Nishidate, F. R., Vandressen, J., Andrade, G., & Nogueira, M. A. (2007). Root Mycorrhizal Colonization and Plant Responsiveness Are Related to Root Plasticity, Soil Fertility and Successional Status of Native Woody Species in Southern Brazil. Journal of Tropical Ecology, 23, 53-62.
http://dx.doi.org/10.1017/S0266467406003713
[70] Zar, J. H. (2009). Biostatistical Analysis (5th ed.). Englewoods Cliffs, NJ: Prentice Hall Inc.

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