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Fig. 3.34 Leaf-cutter ants

Leaf-cutter ants are a special case because they collect an enormous amount of plant biomass and carry it into complicated underground chamber systems where they cultivate fungi. Some quantitative data are compiled in Table 3.3. The loss of foliage by the host plants of up to 40% can reduce their fitness. However, there is also compensatory feedback. Leaf-cutter ants prefer to collect leaf pieces from the upper canopy. Partial defoliation causes an increase in the frequency and variability of light flecks and may result in higher rates of photosynthesis due to increased light penetration and incident irradiance on the remaining parts of tree crowns. Thus, herbivory by leaf-cutter ants appears to have little effect on whole forest canopy photosynthesis although it may considerably reduce photosynthesis locally. The effects on nutrient flow in the forests are patchy because the ants, Atta colombica as the species of the case study of Wirth et al. (2003), bury the nitrogen rich exhausted fungal substrate or refuse from their fungi gardens in large refuse chambers below the fungus chambers of their nests at a depth of 7 m below the surface and only partially on the soil surface. Only deep rooting trees may have access to the former but fine roots of nearby plants may penetrate the latter. The refuse is enriched in nitrogen because the ants prefer to collect the more N-rich young leaves and use more the carbon than the nitrogen. The carbon/nitrogen ratios are 22 in canopy foliage and 36 in normal leaf litter, 21 in the leaf harvest of the ants and only 16 in the refuse dump from the ant's fungi gardens. In the study area of Wirth et al. (2003) on Barro Colorado Island, Panamá, in locations covering less than 0.5% of the area populated by leaf-cutting ants nitrogen flux is therefore about 20 - 30 times higher than in the rest of the forest. Hence, while a large scale benefit of plant nutrition from leaf-cutter ants is debatable local positive effects on plant growth and fitness are evident.

3.4.4.2 Nutrient Partitioning

Different partitioning of inorganic nitrogen assimilation between the roots and shoots of trees is observed in pioneer and mature phase trees of tropical forests. In gaps the mineralization of a large mass of fresh litter, e.g. from fallen trees, may lead to higher availability of NO--N (not NH+-N) and PO4-P (Denslow et al. 1998). Thus, rapidly growing pioneer or colonizing tree species, which are exposed to high irradiation, exhibit a large capacity to assimilate nitrate in their leaves, where light energy can be directly used in photosynthetic nitrate reduction (Aidar et al. 2003). Partitioning of NO--assimilation between roots and shoots is strongly related with average daily photosynthetically active radiation rather than the availability of NO-in the soil (Stewart et al. 1992). Leaves of shaded species have low levels of nitrate reductase and show little capacity to utilize nitrate, even when it was readily available, and primarily assimilate ammonia (Stewart et al. 1988, 1990; Fredeen et al. 1991; Fredeen and Field 1992; Denslow et al. 1998).

3.4.4.3 Flushing of New Leaves and Longevity of Mature Leaves Related to Nutrient Budgets

An interesting phenomenon, which may also be related to nutrient budgets is leaf flushing. New leaves and shoots expand from their buds very rapidly to attain a size close to that of mature leaves, much before they reach their final rigidity and pigmentation. In fact they hang down from the branches as if wilted, and often are coloured brightly yellow or red (Fig. 3.35). The development of chloroplasts and the photosynthetic apparatus is delayed which are both particularly nitrogen-demanding. This can be considered to be an adaptation to conditions of high fungal and herbivore damage to the expanding leaves. Damage may be 100 times higher to young than to mature leaves. Mature leaves are better protected (Kursar and Co-ley 1992a,b; Schlindwein et al. 2006). Costs of damage to the newly flushed leaves remains low since not so many resources have been invested in them. Resource allocation to leaves becomes beneficial when they mature and establish photosynthetic productivity in return. Delayed greening is observed in many species (Kursar and Coley 1992b; Miyazawa and Terashima 2001) and occurs mainly in shade tolerant species and not in gap-requiring species. In the shade a late development of photosynthesis is less disadvantageous than in high light (Kursar and Coley 1992b). It would be interesting to know if the bright colour of freshly flushed leaves even functions in attracting herbivores to these "cheap" leaves, thus protecting the "expensive" mature leaves. In a tropical dry-deciduous forest and a dry-thorn forest in India, phenological strategies have also been observed in relation to leaf flushing. Flushing occurs in the dry season and reaches a peak before the onset of the rains. Herbivorous insects emerge with the rains and attain a peak biomass during the wet months, so that early leaf flushing and maturation provides protection (Murali and Sukumar 1993).

Nutrient availability also affects the structure and longevity of leaves of forest trees. Leaf longevity may vary in different tropical forest tree species from about

Fig. 3.35A,B Leaf-flushing. A in a mango tree, B in Brownea sp.

18 months to several years (Richards 1996). It is highly plastic and can respond to light (Osada et al. 2001). Small leathery leaves ("scleromorphic microphylls") are developed on infertile soils due to N- but mainly P-deficiency (Medina and Cuevas 1989; Medina et al. 1990). Such leaves are more durable and better protected from herbivory (Choong et al. 1992) than large, thin leaves. Thus, nutrient investment in leaf structure provides a return in the form of photosynthetic products for a longer period of time. Deciduous and evergreen species coexist in tropical dry forests. They differ greatly in their investments of resources for leaf construction and maintenance. In deciduous species, with roots occurring under relatively nutrient-rich conditions, leaves can have a potentially high nitrogen-use efficiency (CO2-assimilation related to leaf N-content; see Sect. 4.1.2). Conversely, in evergreen species with lower nitrogen-use efficiency, the long residence time of nitrogen is favourable because roots occur in nutrient-poor soil microhabitats (Sobrado 1991). Both deciduous and evergreen species preserve nitrogen resources. Reserves of nitrogen are maintained in the twigs in drought-deciduous species and in the older leaves in evergreen species, providing some nitrogen for the reconstruction of new leaves following drought and during leaf exchange respectively (Sobrado 1995). In conclusion, plant species obviously allocate resources either to obtain a high photosynthetic assimilation rate from large and fragile leaves for a brief time or to provide a resistant physical structure which results in a lower rate of CO2 assimilation over a longer time (Reich et al. 1991). Thus, mineral nutrition influences the lifespan of leaves.

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