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Nutrient-uptake and -use efficiency in seedlings of rain-forest trees in New Caledonia: monodominants vs. subordinates and episodic vs. continuous regenerators

Published online by Cambridge University Press:  25 July 2018

Jennifer Read*
Affiliation:
School of Biological Sciences, Monash University, Victoria 3800, Australia
Stéphane McCoy
Affiliation:
Environmental Conservation Service, Vale New Caledonia, BP 218 Nouméa, 98845 New Caledonia
Tanguy Jaffré
Affiliation:
AMAP, IRD, CIRAD, CNRS, INRA, Université de Montpellier, Herbarium NOU, BP A5 Nouméa, 98800 New Caledonia
Murray Logan
Affiliation:
Australian Institute of Marine Science, PMB No 3, Townsville MC, Qld 4810, Australia
*
*Corresponding author. Email: [email protected]

Abstract:

The upper canopy of some rain forests in New Caledonia is dominated by single species. These monodominants are commonly secondary species, their dominance not persisting without disturbance. We tested whether dominance is associated with efficient uptake and use of nutrients (N, P and K), comparing between seedlings of monodominants (Nothofagus spp., Arillastrum gummiferum and Cerberiopsis candelabra) and 14 subordinates, grown in a nursery house. We also tested whether this trend applies more broadly to shade-intolerant trees that regenerate episodically (ER species) versus shade-tolerant trees that regenerate continuously (CR species). In the sun treatment, monodominants had higher photosynthetic nutrient-use efficiency and productivity for N and K, and uptake efficiency for N, P and K, than subordinates; ER species had higher photosynthetic nutrient-use efficiency for N, P and K, and uptake efficiency for N and P, than CR species. Uptake efficiency and productivity per nutrient mass were uncorrelated across species, yet Nothofagus spp., A. gummiferum and C. candelabra combined high levels of both traits for N, and Nothofagus spp. and A. gummiferum combined moderate to high levels for P, in sun-grown seedlings. This trait combination may contribute substantially to competitiveness and post-disturbance dominance on these nutrient-poor soils.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2018 

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References

LITERATURE CITED

AERTS, R. & CHAPIN, F. S. 2000. The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances in Ecological Research 30:167.Google Scholar
ALVAREZ-CLARE, S., MACK, M. C. & BROOKS, M. 2013. A direct test of nitrogen and phosphorus limitation to net primary productivity in a lowland tropical wet forest. Ecology 94:15401551.Google Scholar
AMIR, H., LAGRANGE, A., HASSAÏNE, N. & CAVALOC, Y. 2013. Arbuscular mycorrhizal fungi from New Caledonian ultramafic soils improve tolerance to nickel of endemic plant species. Mycorrhiza 23:585595.Google Scholar
BAILEY, R. L. & DELL, T. R. 1973. Quantifying diameter distributions with the Weibull function. Forest Science 19:97104.Google Scholar
BAKER, A. J. M. 1987. Metal tolerance. New Phytologist 106:93111.Google Scholar
BECQUER, T., BOURDON, E. & PETARD, J. 1995. Disponibilité du nickel le long d'une toposéquence de sols développés sur roches ultramafiques de Nouvelle-Calédonie. Comptes rendus de l'Académie des Sciences Série 2a 321:585592.Google Scholar
BECQUER, T., RIGAULT, F. & JAFFRÉ, T. 2002. Nickel bioavailability assessed by ion exchange resin in the field. Communications in Soil Science and Plant Analysis 33:439450.Google Scholar
BERENDSE, F. 1994. Competition between plant populations at low and high nutrient supplies. Oikos 71:253260.Google Scholar
BERENDSE, F. & AERTS, R. 1987. Nitrogen-use-efficiency: a biologically meaningful definition? Functional Ecology 1:293296.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
BROOKSHIRE, E. N. J. & THOMAS, S. A. 2013. Ecosystem consequences of tree monodominance for nitrogen cycling in lowland tropical forest. PLoS ONE 8:e70491. doi: 10.1371/journal.pone.0070491Google Scholar
BURSLEM, D. F. R. P., TURNER, I. M. & GRUBB, P. J. 1994. Mineral nutrient status of coastal hill dipterocarp forest and adinandra belukar in Singapore: bioassays of nutrient limitation. Journal of Tropical Ecology 10:579599.Google Scholar
BURSLEM, D. F. R. P., GRUBB, P. J. & TURNER, I. M. 1995. Responses to nutrient addition among shade-tolerant tree seedlings of lowland tropical rain forest in Singapore. Journal of Ecology 83:113122.Google Scholar
CANHAM, C. D., BERKOWITZ, A. R., KELLY, V. R., LOVETT, G. M., OLLINGER, S. V. & SCHNURR, J. 1996. Biomass allocation and multiple resource limitation in tree seedlings. Canadian Journal of Forest Research 26:15211530.Google Scholar
CHATAIN, A., READ, J. & JAFFRÉ, T. 2009. Does leaf-level nutrient-use efficiency explain Nothofagus-dominance of some tropical rain forests in New Caledonia? Plant Ecology 201:5166.Google Scholar
CHUYONG, G. B., NEWBERY, D. M. & SONGWE, N. C. 2000. Litter nutrients and retranslocation in a central African rain forest dominated by ectomycorrhizal trees. New Phytologist 148:493510.Google Scholar
CONNELL, J. H. & LOWMAN, M. D. 1989. Low-diversity tropical rain forests: some possible mechanisms for their existence. American Naturalist 134:88119.Google Scholar
CORRALES, A., MANGAN, S. A., TURNER, B. L. & DALLING, J. W. 2016. An ectomycorrhizal nitrogen economy facilitates monodominance in a neotropical forest. Ecology Letters 19:383392.Google Scholar
CORRÊA, A., GUREVITCH, J., MARTINS-LOUÇÃO, M. A. & CRUZ, C. 2012. C allocation to the fungus is not a cost to the plant in ectomycorrhizae. Oikos 121:449463.Google Scholar
DEMENOIS, J., IBANEZ, T., READ, J. & CARRICONDE, F. 2017. Comparison of two monodominant species in New Caledonia: floristic diversity and ecological strategies of Arillastrum gummiferum (Myrtaceae) and Nothofagus aequilateralis (Nothofagaceae) rain forests. Australian Journal of Botany 65:1121.Google Scholar
FINLAY, R. D. & READ, D. J. 1986. The structure and function of the vegetative mycelium of ectomycorrhizal plants. II. The uptake and distribution of phosphorus by mycelial strands interconnecting host plants. New Phytologist 103:157165.Google Scholar
GAUTHIER, D., JAFFRÉ, T. & PRIN, Y. 2000. Abundance of Frankia from Gymnostoma spp. in the rhizosphere of Alphitonia neocaledonica, a non-nodulated Rhamnaceae endemic to New Caledonia. European Journal of Soil Biology 36:169175.Google Scholar
GLEASON, S., READ, J., ARES, A. & METCALFE, D. J. 2009. Phosphorus economics of tropical rainforest species and stands across soil contrasts in Queensland, Australia: understanding the effects of soil specialization and trait plasticity. Functional Ecology 23: 11571166.Google Scholar
GLEASON, S. M., READ, J. & ARES, A. 2011. Biomass allocation and phosphorus economics of rain-forest tree seedlings: effects of fertilization and radiation on soil specialists and soil generalists. Journal of Tropical Ecology 27:147161.Google Scholar
GOURMELON, V., MAGGIA, L., POWELL, J. R., GIGANTE, S., HORTAL, S., GUEUNIER, C., LETELLIER, K. & CARRICONDE, F. 2016. Environmental and geographical factors structure soil microbial diversity in New Caledonian ultramafic substrates: a metagenomic approach. PLoS ONE 11 (12): e0167405.Google Scholar
GÜSEWELL, S. 2004. N:P ratios in terrestrial plants: variation and functional significance. New Phytologist 164:243266.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.Google Scholar
HOPE, G. & PASK, J. 1998. Tropical vegetation change in the late Pleistocene of New Caledonia. Palaeogeography, Palaeoclimatology, Palaeoecology 142:121.Google Scholar
HOTHORN, T., BRETZ, F. & WESTFALL, P. 2008. Simultaneous inference in general parametric models. Biometrical Journal 50:346363.Google Scholar
HUNT, R. 2003. Growth analysis, individual plants. Pp. 579588 in Thomas, B., Murphy, D. J. & Murray, D. (eds). Encyclopaedia of applied plant sciences. Academic Press, London.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
IBANEZ, T., MUNZINGER, J., DAGOSTINI, G., HEQUET, V., RIGAULT, F., JAFFRÉ, T. & BIRNBAUM, P. 2014. Structural and floristic characteristics of mixed rainforest in New Caledonia: new data from the New Caledonian Plant Inventory and Permanent Plot Network (NC-PIPPN). Applied Vegetation Science 17:386397.Google Scholar
ISNARD, S., L'HUILLIER, L., RIGAULT, F. & JAFFRÉ, T. 2016. How did the ultramafic soils shape the flora of the New Caledonian hotspot? Plant and Soil 403:5376.Google Scholar
JAFFRÉ, T. 1977. Accumulation du manganèse par des espèces associées aux terrains ultrabasiques de Nouvelle Calédonie. Comptes rendus de l'Académie des Sciences, Série D (Sciences naturelles) 284:15731575.Google Scholar
JAFFRÉ, T., RIGAULT, F. & MUNZINGER, J. 2012. La vegetation. Pp. 77–80 in Bonvallot, J., Gay, J.-C. & Habert, É. (eds). Atlas de la Nouvelle-Calédonie. IRD-Congrès de la Nouvelle-Calédonie, Marseille-Nouméa, 269 pp.Google Scholar
JAFFRÉ, T., PILLON, Y., THOMINE, S. & MERLOT, S. 2013. The metal hyperaccumulators from New Caledonia can broaden our understanding of nickel accumulation in plants. Frontiers in Plant Science. doi: 10.3389/fpls.2013.00279.Google Scholar
JONES, M. D., DURALL, D. M. & TINKER, P. B. 1998. A comparison of arbuscular and ectomycorrhizal Eucalyptus coccifera: growth response, phosphorus uptake efficiency and external hyphal production. New Phytologist 140:125134.Google Scholar
JOURAND, P., HANNIBAL, L., MAJOREL, C., MENGANT, S., DUCOUSSO, M. & LEBRUND, M. 2014. Ectomycorrhizal Pisolithus albus inoculation of Acacia spirorbis and Eucalyptus globulus grown in ultramafic topsoil enhances plant growth and mineral nutrition while limits metal uptake. Journal of Plant Physiology 171:164172.Google Scholar
KRÄMER, U. 2010. Metal hyperaccumulation in plants. Annual Review of Plant Biology 61:517534.Google Scholar
L'HUILLIER, L. & EDIGHOFFER, S. 1996. Extractability of nickel and its concentration in cultivated plants in Ni rich ultramafic soils of New Caledonia. Plant and Soil 186:255–26.Google Scholar
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
MCCOY, S. 1991. Edaphic controls influencing the distribution of Nothofagus aequilateralis on ultrabasic soils at the Col de Mouirange, New Caledonia. Honours Dissertation, Australian National University.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.Google Scholar
MCGUIRE, K. L. 2007. Common ectomycorrhizal networks may maintain monodominance in a tropical rain forest. Ecology 88:567574.Google Scholar
MCGUIRE, K. L., ZAK, D. R., EDWARDS, I. P., BLACKWOOD, C. B. & UPCHURCH, R. 2010. Slowed decomposition is biotically mediated in an ectomycorrhizal, tropical rain forest. Oecologia 164: 785795.Google Scholar
MORAT, P., JAFFRÉ, T., TRONCHET, F., MUNZINGER, J., PILLON, Y., VEILLON, J.-M. & CHALOPIN, M. 2012. Le référentiel taxonomique Florical et les caractéristiques de la flore vasculaire indigène de la Nouvelle-Calédonie. Adansonia, sér. 3 34 (2):179221.Google Scholar
NEBA, G. A., NEWBERY, D. M. & CHUYONG, G. B. 2016. Limitation of seedling growth by potassium and magnesium supply for two ectomycorrhizal tree species of a Central African rain forest and its implication for their recruitment. Ecology and Evolution 6: 125142.Google Scholar
NEWBERY, D. M. 2005. Ectomycorrhizas and mast fruiting in trees: linked by climate-driven tree resources? New Phytologist 167:324326.Google Scholar
NEWBERY, D. M., ALEXANDER, I. J. & ROTHER, J. A. 1997. Phosphorus dynamics in a lowland African rain forest: the influence of ectomycorrhizal trees. Ecological Monographs 67:367409.Google Scholar
NEWBERY, D. M., CHUYONG, G. B., GREEN, J. J., SONGWE, N. C., TCHUENTEU, F. & ZIMMERMANN, L. 2002. Does low phosphorus supply limit seedling establishment and tree growth in groves of ectomycorrhizal trees in a Central African Rainforest? New Phytologist 156:297311.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., 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
OLDE VENTERINK, H., WASSEN, M. J., VERKROOST, A. W. M. & DE RUITER, P. C. 2003. Species richness-productivity patterns differ between N-, P-, and K-limited wetlands. Ecology 84: 21912199.Google Scholar
PAOLI, G. D. & CURRAN, L. M. 2007. Soil nutrients limit fine litter production and tree growth in lowland tropical rain forest of southwestern Borneo. Ecosystems 10:503518.Google Scholar
PAOLI, G. D., CURRAN, L. M. & ZAK, D. R. 2005. Phosphorus efficiency of Bornean rain forest productivity: evidence against the unimodal efficiency hypothesis. Ecology 86:15481561.Google Scholar
PEH, K. S.-H., LEWIS, S. L. & LLOYD, J. 2011a. Mechanisms of monodominance in diverse tropical tree-dominated systems. Journal of Ecology 99:891898.Google Scholar
PEH, K. S.-H., SONKÉ, B., LLOYD, J., QUESADA, C. A. & LEWIS, S. L. 2011b. Soil does not explain monodominance in a Central African tropical forest. PLoS ONE 6 (2): e16996. doi: 10.1371/journal.pone.0016996.Google Scholar
PEH, K. S.-H., SONKE, B., TAEDOUNG, H., SENE, O., LLOYD, J. & LEWIS, S. L. 2012. Investigating diversity dependence of tropical forest litter decomposition: experiments and observations from Central Africa. Journal of Vegetation Science 23:223235.Google Scholar
PERRIER, N., COLIN, F., JAFFRÉ, T., AMBROSI, J.-P., ROSE, J. & BOTTERO, J.-Y. 2004. Nickel speciation in Sebertia acuminata, a plant growing on a lateritic soil of New Caledonia. Comptes Rendus Geoscience 336:567577.Google Scholar
PERRIER, N., AMIR, H. & COLIN, F. 2006. Occurrence of mycorrhizal symbioses in the metal-rich lateritic soils of the Koniambo Massif, New Caledonia. Mycorrhiza 16:449458.Google Scholar
PINHEIRO, J. C. & BATES, D. M. 2000. Mixed-effects models in S and S-PLUS. Springer-Verlag, New York. 528 pp.Google Scholar
PLASSARD, C. & DELL, B. 2010. Phosphorus nutrition of mycorrhizal trees. Tree Physiology 30:11291139.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. Population 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., FERRIS, J. M. & JAFFRÉ, T. 2002. Foliar mineral content of Nothofagus species on ultramafic soils in New Caledonia and non-ultramafic soils in Papua New Guinea. Australian Journal of Botany 50:607617.Google Scholar
READ, J., JAFFRÉ, T., FERRIS, J. M., MCCOY, S. & HOPE, G. S. 2006. 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
READ, J., EVANS, R., SANSON, G. D., KERR, S. & JAFFRÉ, T. 2011. Wood properties and trunk allometry of co-occurring rainforest canopy trees in a cyclone-prone environment. American Journal of Botany 98:17621772.Google Scholar
READ, J., MCCOY, S. & JAFFRÉ, T. 2015. Shade-tolerance of seedlings of rain-forest trees: monodominants vs. subordinates and episodic vs. continuous regenerators. Journal of Tropical Ecology 31: 541552.Google Scholar
READ, J., MCCOY, S., JAFFRÉ, T., SANSON, G. & LOGAN, M. 2017. Growth and biomass allocation in seedlings of rain-forest trees in New Caledonia: monodominants vs. subordinates and episodic vs. continuous regenerators. Journal of Tropical Ecology 33: 128142.Google Scholar
REICH, P. B., UHL, C., WALTERS, M. B. & ELLSWORTH, D. S. 1991. Leaf lifespan as a determinant of leaf structure and function among 23 amazonian tree species. Oecologia 86:1624.Google Scholar
TIBBETT, M. & SANDERS, F. E. 2002. Ectomycorrhizal symbiosis can enhance plant nutrition through improved access to discrete organic nutrient patches of high resource quality. Annals of Botany 89:783789.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
VITOUSEK, P. M., PORDER, S., HOULTON, B. Z. & CHADWICK, O. A. 2010. Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecological Applications 20:515.Google Scholar
WRIGHT, S. J., YAVITT, J. B., WURZBURGER, N., TURNER, B. L., TANNER, E. V. J., SAYER, E. J., SANTIAGO, L. S., KASPARI, M., HEDIN, L. O., HARMS, K. E., GARCIA, M. N. & CORRE, M. D. 2011. Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. Ecology 92:16161625.Google Scholar