CASE STUDY 16.3  Rainforest succession and nitrogen nutrition

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M.H. Turnbull

Nitrogen (N) is a key limiting nutrient in natural ecosystems, partly because plants have a high requirement, but mostly because readily available forms are often in short supply (Case study 16.2). Foliage commonly contains high concentrations of N (1–5% of dry mass) and meeting this need is a major energy-requiring process because N uptake by plants and N assimilation within plants are both metabolically expensive (Chapin et al. 1987).

Energy requirement is especially high if nitrate is the sole source of N because biological reduction of nitrate ions and subsequent incorporation into plant N metabolism has a higher requirement for both ATP and reductant than does direct use of ammonium compounds. Much of this energy comes via energy transduction from sunlight, and under light conditions which limit growth (e.g. forest understorey) nitrate assimilation in leaves must compete with other synthetic events for biological forms of energy derived from chloroplasts.

In high light environments, excess ATP and reductant from photosynthetic energy transduction (Section 1.2) can be used in leaves for photoreduction of the nitrate that reaches transpiring leaves via xylem flow. Light-dependent reduction of nitrate in leaves is less costly in energy terms than nitrate reduction in roots (Raven 1985), so that some selective advantage is derived from a leaf-based system for nitrate reduction provided solar radiation is abundant.

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Figure 1 Nitrate reductase activity in leaves of three Mexican species of Piper varies according to their sun/shade adaptation and cultural conditions. Piper auritum colonises disturbance gaps in rainforest at Los Tuxtlas and shows the highest levels; P. aequale is a shade-tolerant species adapted to understorey habitats, and shows the lowest levels of nitrate reductase; P. hispidum is a generalist species and shows an intermediate level of nitrate reductase activity. (Based on Fredeen and Field 1996)

Accordingly, pioneer and gap species that are sunloving (Section 12.1.3) express levels of nitrate reductase activity that are 5–20 times those of understorey species in both Australian rainforests (Stewart et al. 1988) and Mexican communities (Figure 1; Fredeen and Field 1992).

Nitrate reductase activity of pioneer species is located primarily in leaves, and in line with sun/shade adaptation this prime site appears to be genetically set rather than environmentally driven. Leaf activity is none the less modulated by light because nitrate reductase activity in shoots becomes even more pronounced compared with roots with increased photon irradiance, and especially in conditions where photosynthesis is light saturated. By implication, nitrate reduction is an energy-effective mechanism for N assimilation by sunloving plants in strong light on open areas or in major disturbance gaps of forests.

As a consequence of their high leaf nitrate reductase activities, early-successional (pioneer) species are well placed to take advantage of soil nitrate from disturbed sites such as large gaps or along forest edges. Warm soils in those places could also favour nitrification via temperature-driven microbial activity. An important implication of the very low nitrate reductase activities in species of later-successional stages of forest development is that these species are likely to be using a source of N other than nitrate such as ammonium and complex organic N compounds.

One further advantage of a nutritional strategy involving leaf nitrate reduction at high photon irradiance in pioneer/gap species comes from dissipation of excess photochemical energy that might otherwise contribute to photoinhibition (Smirnoff and Stewart 1985; Section 12.1.2).

Mycorrhizas and plant access to organic nitrogen

Nitrate N is widely recognised as a key source for sunloving (early-successional) plants on disturbed sites, but soil nitrate is less abundant during later-successional stages of rainforest dynamics or in long-established and undisturbed communities. However, complex organic forms of N together with unmineralised ammonium compounds do abound, raising a question as to their availability for plant growth. Some plants are long known to show a distinct preference for ammonium over nitrate ions as an N source; less known is the ability of mycorrhizal associations to extend the nutrient base of their host plants even further to include organic forms of N.

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Figure 2 Seedlings of Eucalyptus grandis (a) and E. maculata (b) benefit greatly from ectomycorrhizal association when dependent on organic N as a sole source of external N. Growth on nitrate N or ammonium N was not enhanced by fungal infection. Open bars refer to non-mycorrhizal seedlings, solid bars refer to seedlings grown in association with Elaphomyces sp. Abbreviations beneath histograms refer to N sources where -N denotes a nitrogen-free medium; NO3 = nitrate; NH4 = ammonium; ARG = arginine; ASN = asparagine; GLN = glutamine; HIS = histidine; BSA = bovine serum albumen. (Based on Turnbull et al. 1995)

Mycorrhizal fungi feature prominently in the P nutrition of their host plants, and especially on impoverished sites (Sections 5.3.4 and 16.4.1) but their significance for N nutrition is less clear. In growth experiments with seedlings of Eucalyptus spp. (Botany Department, University of Queensland) non-mycorrhizal plants in sterile culture grew poorly on organic N. By contrast, ectomycorrhizal infection enabled seedlings to use organic sources of N and they grew much faster. Infected plants grew well on a range of amino acids and even on protein N (Figure 2). This capacity to use a broad spectrum of organic sources has important implications for tree seedling nutrition. In field situations, a number of N sources might thus be available despite their low concentrations. This presumed ability to access a diversity of N sources might confer distinct nutritional advantages on mycorrhizal plants in forest ecosystems.

When mycorrhizal seedlings of Eucalyptus grandis were offered a mixed source of N in the growth medium, they derived 50% of total N from the amino acid asparagine and 40% from albumen protein (Turnbull et al. 1996). Organic sources of N may thus be significant to mycorrhizal plants even in the presence of readily assimilable inorganic ions, especially where plants must scavenge for sparse resources. However, it would be misleading to suggest that only those plants with a fungal compatibility are able to utilise organic sources of nitrogen directly. We now know that obligately non-mycorrhizal species such as Hakea sp. from coastal heathland in Australia (Turnbull et al. 1996) and Eriophorum vaginatum from arctic tundra (Chapin et al. 1993) can also incorporate labelled amino acid sources. Clearly, some plants are able to short-circuit the mineralisation cycle commonly viewed as the sole source of usable N, either directly or via symbiotic association.

Taken overall, flexibility in N nutrition ensures that a selective advantage during colonisation on a disturbed site where nitrate N predominates is not lost as forests mature and nitrate N is replaced by ammonium N and more complex forms of organic N.

References

Chapin, F.S., III, Bloom, A.J., Field, C.B. and Waring, R.H. (1987). ‘Plant responses to multiple environmental factors’, BioScience, 37, 49–57.

Chapin F.S, III, Moilanen, L. and Kielland, K. (1993). ‘Preferential use of organic nitrogen for growth by a non-mycorrhizal arctic sedge’, Nature, 361, 150–153.

Fredeen, A.L. and Field, C.B. (1992). ‘Ammonium and nitrate uptake in gap, generalist, and understorey species of the genus Piper’, Oecologia, 92, 207–214.

Fredeen, A.L. and Field, C.B. (1996) ‘Ecophysiological constraints on the distribution of Piper species’, in Tropical Forest Plant Ecophysiology, eds S.S. Mulkey, R.L. Chazdon and A.P. Smith, 597–618, Chapman and Hall: New York.

Raven, J.A. (1985). ‘Regulation of pH and osmolarity generation in vascular land plants: costs and benefits in relation to efficiency of use of water, energy and nitrogen’, New Phytologist, 101, 25–77.

Smirnoff, N. and Stewart, G.R. (1985). ‘Nitrate assimilation and translocation by higher plants: comparative physiology and ecological consequences’, Physiologia Plantarum, 64, 133–140.

Stewart, G.R., Hegarty, E. and Specht, R.L. (1988). ‘Inorganic nitrogen assimilation in plants of Australian rainforest communities’, Physiologia Plantarum, 74, 26–33.

Turnbull, M.H., Goodall, R. and Stewart, G.R. (1995). ‘The impact of mycorrhizal colonisation upon nitrogen source acquisition and metabolism in seedlings of Eucalyptus grandis Hill ex Maiden and Eucalyptus maculata Hook’, Plant, Cell and Environment, 18, 1386–1394.

Turnbull, M.H., Schmidt, S., Erskine, P.D., Richards, S. and Stewart, G.R. (1996). ‘Root adaptation and nitrogen source acquisition in natural ecosystems’, Tree Physiology, 16, 941–948.

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