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Shade-tolerance of seedlings of rain-forest trees: monodominants vs. subordinates and episodic vs. continuous regenerators

Published online by Cambridge University Press:  09 October 2015

Jennifer Read*
Affiliation:
School of Biological Sciences, Monash University, Victoria 3800, Australia
Stéphane McCoy
Affiliation:
Environmental Conservation Service, Vale New Caledonia, BP 218 Noumea 98845, New Caledonia
Tanguy Jaffré
Affiliation:
UMR AMAP, IRD – Institut de recherche pour le développement, Laboratoire de Botanique et d’Ecologie Végétale Appliquées, Herbarium NOU, BP A5 Noumea 98848, New Caledonia
*
1 Corresponding author. Email: jenny.read@monash.edu

Abstract:

Several monodominant rain-forest trees in New Caledonia have population size structures suggesting establishment following large-scale disturbance, with eventual replacement by shade-tolerant species predicted in the absence of future disturbance. Links of dominance and population dynamics to leaf-level photosynthesis were investigated in seedlings of 20 tree species from these forests, grown in experimental sun and shade conditions. In particular, we tested whether episodically regenerating (ER) species, including monodominants, have higher assimilation rates at high irradiances and lower tolerance of shade than continuously regenerating species (CR). ER species had higher maximum net assimilation rates (Amax-area) in sun plants (9.6 ± 0.4 μmol m−2 s−1) than CR species (6.2 ± 0.3 μmol m−2 s−1) and high plasticity, typical of shade-intolerant species, but monodominant species did not differ from other ER species. CR species had leaf-level traits consistent with shade tolerance, including lower dark respiration rates (Rd-area = 0.47 ± 0.03μmol m−2 s−1; Rd-mass = 7 ± 1 nmol g−1 s−1) than ER species (Rd-area = 0.63 ± 0.06 μmol m−2 s−1; Rd-mass = 11 ± 2 nmol g−1 s−1) in shade plants. Hence leaf-level assimilation traits were largely consistent with regeneration patterns, but do not explain why some shade-intolerant species can achieve monodominance.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2015 

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References

LITERATURE CITED

ANDERSON, J. A. R. 1964. Observations on climatic damage in peat swamp forest in Sarawak. Empire Forestry Review 43:145158.Google Scholar
AUGSPURGER, C. K. 1984a. Light requirements of neotropical tree seedlings: a comparative study of growth and survival. Journal of Ecology 72:777795.Google Scholar
AUGSPURGER, C. K. 1984b. Seedling survival of tropical tree species: interactions of dispersal distance, light-gaps, and pathogens. Ecology 65:17051712.Google Scholar
BAILEY, R. L. & DELL, T. R. 1973. Quantifying diameter distributions with the Weibull function. Forest Science 19:97104.Google Scholar
BALTZER, J. L. & THOMAS, S. C. 2007. Determinants of whole-plant light requirements in Bornean rain forest tree saplings. Journal of Ecology 95:12081221.Google Scholar
BAZZAZ, F. A. 1979. The physiological ecology of plant succession. Annual Review of Ecology and Systematics 10:351371.CrossRefGoogle Scholar
BJÖRKMAN, O. 1981. Responses to different quantum flux densities. Pp. 57107 in Lange, O. L., Nobel, P. S., Osmond, C. B. & Zeigler, H. (eds). Physiological plant ecology. New Series, Volume 12A. Springer-Verlag, Berlin.Google Scholar
BOARDMAN, N. K. 1977. Comparative photosynthesis of sun and shade plants. Annual Review of Plant Physiology 28:355377.Google Scholar
BREARLEY, F. Q., PRESS, M. C. & SCHOLES, J. D. 2003. Nutrients obtained from leaf litter can improve the growth of dipterocarp seedlings. New Phytologist 160:101110.Google Scholar
CANHAM, C. D., FINZI, A. C., PACALA, S. W. & BURBANK, D. H. 1994. Causes and consequences of resource heterogeneity in forests – interspecific variation in light transmission by canopy trees. Canadian Journal of Forest Research 24:337349.Google Scholar
CANHAM, C. D., KOBE, R. K., LATTY, E. F. & CHAZDON, R. L. 1999. Interspecific and intraspecific variation in tree seedling survival: effects of allocation to roots versus carbohydrate reserves. Oecologia 121:111.Google Scholar
CLARKE, K. R. 1993. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18:117143.Google Scholar
CLARKE, K. R. & GORLEY, R. N. 2006. PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth. 192 pp.Google Scholar
CONNELL, J. H. & LOWMAN, M. D. 1989. Low-diversity tropical rain forests: some possible mechanisms for their existence. American Naturalist 134:88119.CrossRefGoogle Scholar
CRAINE, J. M. & REICH, P. B. 2005. Leaf-level light compensation points in shade-tolerant woody seedlings. New Phytologist 166:710713.Google Scholar
DAVIES, S. J. 1998. Photosynthesis of nine pioneer Macaranga species from Borneo in relation to life history. Ecology 79:22922308.Google Scholar
EGGELING, W. J. 1947. Observations on the ecology of the Budongo rain forest, Uganda. Journal of Ecology 34:2087.Google Scholar
GIVNISH, T. J. 1988. Adaptation to sun and shade: a whole-plant perspective. Australian Journal of Plant Physiology 15:6392.Google Scholar
GLEASON, S. M., READ, J. & ARES, A. 2011. Biomass allocation and phosphorus economics of rain-forest tree seedlings: effects of fertilisation and radiation on soil specialists and soil generalists. Journal of Tropical Ecology 27:147161.Google Scholar
GREEN, P. T., HARMS, K. E. & CONNELL, J. H. 2014. Nonrandom, diversifying processes are disproportionately strong in the smallest size classes of a tropical forest. Proceedings of the National Academy of Sciences USA 111:1864918654.Google Scholar
GRUBB, P. J. & METCALFE, D. J. 1996. Adaptation and inertia in the Australian tropical lowland rain-forest flora: contradictory trends in intergeneric and intrageneric comparisons of seed size in relation to light demand. Functional Ecology 10:512520.Google Scholar
HART, T. B. 1990. Monospecific dominance in tropical rain forests. Trends in Ecology and Evolution 5:611.Google Scholar
HEENAN, P. B. & SMISSEN, R. D. 2013. Revised circumscription of Nothofagus and recognition of the segregate genera Fuscospora, Lophozonia, and Trisyngyne (Nothofagaceae). Phytotaxa 146:131.Google Scholar
HENKEL, T. W., MAYOR, J. R. & WOOLLEY, L. P. 2005. Mast fruiting and seedling survival of the ectomycorrhizal, monodominant Dicymbe corymbosa (Caesalpiniaceae) in Guyana. New Phytologist 167:543556.CrossRefGoogle ScholarPubMed
HIDAKA, A. & KITAYAMA, K. 2013. Relationship between photosynthetic phosphorus-use efficiency and foliar phosphorus fractions in tropical tree species. Ecology and Evolution 3:48724880.CrossRefGoogle ScholarPubMed
HORTON, J. L. & NEUFELD, H. S. 1998. Photosynthetic responses of Microstegium vimineum (Trin.) A. Camus, a shade-tolerant, C4 grass, to variable light environments. Oecologia 114:1119.Google Scholar
IBANEZ, T. & BIRNBAUM, P. 2014. Monodominance at the rainforest edge: case study of Codia mackeeana (Cunoniaceae) in New Caledonia. Australian Journal of Botany 62:312321.Google Scholar
JAFFRÉ, T. 1980. Étude écologique du peuplement végétal des sols dérivés de roches ultrabasiques en Nouvelle Calédonie. Collection Travaux et Documents de l’ORSTOM no. 124. ORSTOM, Paris. 273 pp.Google Scholar
JAFFRÉ, T. & VEILLON, J.-M. 1990. Etude floristique et structurale de deux forêts denses humides sur roches ultrabasiques en Nouvelle-Calédonie. Adansonia 3–4:243273.Google Scholar
KITAJIMA, K. 1994. Relative importance of photosynthetic traits and allocation patterns as correlates of seedling shade tolerance of 13 tropical trees. Oecologia 98:419428.CrossRefGoogle ScholarPubMed
KOBE, R. K. 1997. Carbohydrate allocation to storage as a basis of interspecific variation in sapling survivorship and growth. Oikos 80:226233.Google Scholar
KOBE, R. K., PACALA, S. W., SILANDER, J. A. & CANHAM, C. D. 1995. Juvenile tree survivorship as a component of shade tolerance. Ecological Applications 5:517532.Google Scholar
LOACH, K. 1967. Shade tolerance in tree seedlings I. Leaf photosynthesis and respiration in plants raised under artificial shade. New Phytologist 66:607621.Google Scholar
LUSK, C. H. & REICH, P. B. 2000. Relationships of leaf dark respiration with light environment and tissue nitrogen content in juveniles of 11 cold-temperate tree species. Oecologia 123:318329.CrossRefGoogle ScholarPubMed
MANAUTÉ, J., JAFFRÉ, T., VEILLON, J. M. & KRANITZ, M. L. 2009. Review of the Araucariaceae in New Caledonia. Pp. 347358 in Bieleski, R. L. & Wilcox, M. D. (eds.). Proceedings of the 2002 Araucariaceae Symposium, Araucaria-Agathis-Wollemia. International Dendrology Society, Auckland.Google Scholar
MCCARTHY-NEUMANN, S. & KOBE, R. K. 2008. Tolerance of soil pathogens co-varies with shade tolerance across species of tropical tree seedlings. Ecology 89:18831892.Google Scholar
MCCOY, S., JAFFRÉ, T., RIGAULT, F. & ASH, J. E. 1999. Fire and succession in the ultramafic maquis of New Caledonia. Journal of Biogeography 26:579594.CrossRefGoogle Scholar
MONTGOMERY, R. A. & CHAZDON, R. L. 2002. Light gradient partitioning by tropical tree seedlings in the absence of canopy gaps. Oecologia 131:165174.Google Scholar
MORAT, P., JAFFRÉ, T., TRONCHET, F., MUNZINGER, J., PILLON, Y., VEILLON, J.-M. & CHALOPIN, M. 2012. The taxonomic database FLORICAL and characteristics of the indigenous flora of New Caledonia. Adansonia sér. 3 34:179221.Google Scholar
MYERS, J. A. & KITAJIMA, K. 2007. Carbohydrate storage enhances seedling shade and stress tolerance in a neotropical forest. Journal of Ecology 95:383395.Google Scholar
NASCIMENTO, M. T., BARBOSA, R. I., VILLELA, D. M. & PROCTOR, J. 2007. Above-ground biomass changes over an 11-year period in an Amazon monodominant forest and two other lowland forests. Plant Ecology 192:181191.Google Scholar
NEWBERY, D. M, VAN DER BURGT, X. M. & MORAVIE, M.-A. 2004. Structure and inferred dynamics of a large grove of Microberlinia bisulcata trees in central African rain forest: the possible role of periods of multiple disturbance events. Journal of Tropical Ecology 20:131143.Google Scholar
NEWBERY, D. M., PRAZ, C. J., VAN DER BURGT, X. M., NORGHAUER, J. M. & CHUYONG, G. B. 2010. Recruitment dynamics of the grove-dominant tree Microberlinia bisulcata in African rain forest: extending the light response versus adult longevity trade-off concept. Plant Ecology 206:151177.Google Scholar
NEWBERY, D. M., VAN DER BURGT, X. M., WORBES, M., CHUYONG, G. B. 2013. Transient dominance in a central African rain forest. Ecological Monographs 83:339382.Google Scholar
NIINEMETS, U. 2006. The controversy over traits conferring shade-tolerance in trees: ontogenetic changes revisited. Journal of Ecology 94:464470.Google Scholar
OSUNKOYA, O. O., ASH, J. E., HOPKINS, M. S. & GRAHAM, A. W. 1994. Influence of seed size and seedling ecological attributes on shade-tolerance of rain-forest tree species in Northern Queensland. Journal of Ecology 82:149163.Google Scholar
PEARCY, R. W. 1988. Photosynthetic utilisation of lightflecks by understory plants. Australian Journal of Plant Physiology 15:223238.Google Scholar
PEH, K. S.-H., LEWIS, S. L. & LLOYD, J. 2011. Mechanisms of monodominance in diverse tropical tree-dominated systems. Journal of Ecology 99:891898.Google Scholar
PORTSMUTH, A. & NIINEMETS, Ü. 2007. Structural and physiological plasticity in response to light and nutrients in five temperate deciduous woody species of contrasting shade tolerance. Functional Ecology 21:6177.Google Scholar
READ, J. & HOPE, G. S. 1996. Ecology of Nothofagus forests of New Guinea and New Caledonia. Pp. 200256 in Veblen, T. T., Hill, R. S. & Read, J. (eds.). The ecology and biogeography of Nothofagus forests. Yale University Press, New Haven.Google Scholar
READ, J. & JAFFRÉ, T. 2013. Populations dynamics of canopy trees in New Caledonian rain forests: are monodominant Nothofagus (Nothofagaceae) forests successional to mixed rain forests? Journal of Tropical Ecology 29:485499.Google Scholar
READ, J., JAFFRÉ, T., GODRIE, E., HOPE, G. S. & VEILLON, J.-M. 2000. Structural and floristic characteristics of some monodominant and adjacent mixed rainforests in New Caledonia. Journal of Biogeography 27:233250.Google Scholar
READ, J., SANSON, G. D., JAFFRÉ, T. & BURD, M. 2006a. Does tree size influence timing of flowering in Cerberiopsis candelabra (Apocynaceae), a long-lived monocarpic rain forest tree? Journal of Tropical Ecology 22:19.Google Scholar
READ, J., JAFFRÉ, T., FERRIS, J. M., MCCOY, S. & HOPE, G. S. 2006b. Does soil determine the boundaries of monodominant rain forest with adjacent mixed rain forest and maquis on ultramafic soils in New Caledonia? Journal of Biogeography 33:10551065.Google Scholar
READ, J., SANSON, G. D., BURD, M. & JAFFRÉ, T. 2008. Mass flowering and parental death in the regeneration of Cerberiopsis candelabra (Apocynaceae), a long-lived monocarpic tree in New Caledonia. American Journal of Botany 95:558567.Google Scholar
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, S3:S143S164.Google Scholar
RICHARDS, P. W. 1952. The tropical rain forest. (First edition). Cambridge University Press, Cambridge. 450 pp.Google Scholar
ROSS, R. 1954. Ecological studies on the rain forest of southern Nigeria. III. Secondary succession in the Shassa Forest Reserve. Journal of Ecology 42:259282.Google Scholar
STRAUSS-DEBENEDETTI, S. & BAZZAZ, F. A. 1991. Plasticity and acclimation to light in tropical Moraceae of different successional positions. Oecologia 87:377387.Google Scholar
THOMPSON, W. A., STOCKER, G. C. & KRIEDEMANN, P. E. 1988. Growth and photosynthetic response to light and nutrients of Flindersia brayleyana F. Muell., a rain forest tree with broad tolerance to sun and shade. Australian Journal of Plant Physiology 15:299315.Google Scholar
TORTI, S. D., COLEY, P. D. & KURSAR, T. A. 2001. Causes and consequences of monodominance in tropical lowland forests. American Naturalist 157:141153.Google Scholar
TURNER, I. M. 2001. The ecology of trees in the tropical rain forest. Cambridge University Press, Cambridge. 298 pp.Google Scholar
VAARTAJA, O. 1962. The relationship of fungi to survival of shaded tree seedlings. Ecology 43:547549.Google Scholar
VALLADARES, F. & NIINEMETS, Ü. 2008. Shade tolerance, a key plant feature of complex nature and consequences. Annual Review of Ecology, Evolution, and Systematics 39:237257.Google Scholar
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 143:143154.Google Scholar
WALTERS, M. B. & REICH, P. B. 2000. Seed size, nitrogen supply, and growth rate affect tree seedling survival in deep shade. Ecology 81:18871901.Google Scholar
WHITMORE, T. C. 1998. An introduction to tropical rain forests. (Second edition). Oxford University Press, Oxford. 296 pp.Google Scholar