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Leaf Life Span and the Mobility of "Non-Mobile" Mineral Nutrients

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Leaf Life Span and the Mobility of Silva Fennica 36(3) research articles Leaf Life Span and the Mobility of “Non-Mobile’’ Mineral Nutrients – the Case of Boron in Conifers Pedro J. Aphalo, Anna W. Schoettle and Tarja Lehto Aphalo, P.J., Schoettle, A.W. & Lehto T. 2002. Leaf lifespan and the mobility of “non-mobile’’ mineral nutrients – the case of boron in conifers. Silva Fennica 36(3): 671–680. Nutrient conservation is considered important for the adaptation of plants to infertile environments. The importance of leaf life spans in controlling mean residence time of nutrients in plants has usually been analyzed in relation to nutrients that can be retranslocated within the plant. Longer leaf life spans increase the mean residence time of all mineral nutrients, but for non-mobile nutrients long leaf life spans concurrently cause concentrations in tissues to increase with leaf age, and consequently may reduce non-mobile nutrient use effi ciency. Here we analyze how the role of leaf life span is related to the mobility of nutrients within the plant. We use optimality concepts to derive testable hypotheses, and preliminar- ily test them for boron (B), a nutrient for which mobility varies among plant species. We review published and unpublished data and use a simple model to assess the quantitative importance of B retranslocation for the B budget of mature conifer forests and as a mechanism for avoiding toxicity. Keywords boron, conifers, leaf life span, model, needle age, nutrient mobility, toxicity Authors’ addresses Aphalo and Lehto, Faculty of Forestry, University of Joensuu, P.O. Box 111, FIN-80101 Joensuu, Finland; Schoettle, Rocky Mountain Research Station, 240 West Prospect Road, Fort Collins, CO 80526, USA. Current address: Aphalo, Department of Biological and Environmental Science, University of Jyväskylä, P.O. Box 35, FIN-40351 Jyväskylä, Finland Fax +358 14 260 2321 E-mail pedro.aphalo@jyu.fi Received 30 June 2000 Accepted 20 May 2002 1 Introduction was noted by Harper in 1914. According to Eck- stein et al. (1999) nutrients can be conserved Nutrient conservation is considered to be impor- mainly by extending the life span of plant parts tant for the adaptation of plants to infertile envi- or by minimizing the nutrient content of those ronments (Eckstein et al. 1999). The negative parts which are abscised. (In this context it is correlation between the distribution of long leaf important to distinguish between leaf life span life spans and the nutrient availability of habitats and leaf habit, as evergreenness can be achieved 671 Silva Fennica 36(3) research articles by replacement of short lived leaves several times Boron is a plant micronutrient peculiar in two per year, see Kikuzawa 1991.) respects: (1) its mobility varies markedly among However, there are many possible selection plant species, and (2) the range of tissue concen- forces favouring long leaf life spans. Chabot trations spanning from defi ciency to toxicity is and Hicks (1982) list 11 hypothetical advan- narrow. This makes it a very good candidate for tages, and on a world wide basis mineral nutrient testing optimality hypotheses because (1) there is conservation may not be the most widespread. genetic variability, and (2) the selective pressure Furthermore, these advantages are not mutually against suboptimal use is strong. exclusive. Schoettle and Fahey (1994) have In species in which boron moves mainly in reviewed the nature of foliage longevity in pines, the xylem sap it accumulates and concentrations and proposed the ecological light compensation increase as the foliage grows older. In those spe- point as the immediate control on leaf shedding. cies in which at least part of the boron in the Nutrient conservation can be measured through foliage is retranslocated through the phloem to the mean residence time of a nutrient in the plant other tissues (e.g. roots, infl orescences, seeds, (Eckstein et al. 1999). However, plant nutrient- etc.) its concentration in the foliage tends to use effi ciency depends both on mean residence remain constant (see Brown and Shelp 1997). time and nutrient productivity. Nutrient produc- When there is B retranslocation through the tivity relates dry mass production to instantane- phloem, it depends on the formation of complexes ous nutrient content (Berendse and Aerts 1987). with sugar alcohols such as mannitol, sorbitol, Apparently mean residence time and nutrient pro- and possibly pinitol (see Brown and Shelp 1997). ductivity are negatively correlated (see Eckstein Recently B-sorbitol and B-mannitol, and also et al. 1999, and references therein). B-fructose complexes have been demonstrated Plant adaptations and responses to multiple to occur in the phloem sap of B-retranslocating environmental factors are frequently non-additive species (Hu et al. 1997). Further evidence of the (Chapin III et al. 1987). The importance of mean importance of sugar alcohols was obtained from residence time and leaf life span has been dis- transgenic tobacco plants, in which the induction cussed in the literature mainly in relation to the of sorbitol formation gave the new ability to macronutrients N and P, which are mobile in the mobilize B within the plant (Brown et al. 1999). plant, and there is convincing evidence that long Given a long leaf life span (e.g. as adaptation to leaf life spans are in many cases an adaptation low availability of a mobile macronutrient such to low supply of N or P (Reich 1993). However, as nitrogen), optimal use of B when availability only some mineral nutrients are mobile in the plant is low, or toxicity avoidance when availability is (i.e. they can be redistributed) while others are not high, should favour individuals with the ability mobile (i.e. they cannot be redistributed). A long to redistribute B away from ‘old’ foliage and life span of the foliage and concomitant long mean towards growing tissues. residence time improves the use effi ciency only However, boron retranslocation is not the only for mineral nutrients which can be redistributed strategy that may have evolved in plants for within the plant. In contrast, if there is a continu- coping with low or high B availability: grasses ous fl ux of a ‘non-mobile’ nutrient towards the have very low B requirements (Dugger 1983), and foliage a long leaf life span decreases its produc- other species like sunfl ower can tolerate high B tivity, and does not increase use effi ciency. concentrations in their tissues using an unknown For phloem mobile nutrients recycling occurs mechanism to avoid toxicity (Dannel et al. 1999). partly within the plant, and decreases possible However, conifers like most species with long loss through leaching or immobilization in the lived foliage have woody tissues which require soil. In contrast, in the case of nutrients that are B for their structural integrity. not mobile in the plant recycling occurs outside the plant, through the soil, and immobilization can occur by accumulation in old living foliage. In either case use effi ciency increases when over- all immobilization and losses are decreased. 672 Aphalo, Schoettle and Lehto Leaf Life Span and the Mobility of “Non-Mobile” Mineral Nutrients – the Case of Boron in Conifers 2 Hypothesis oldest needles given above, and additionally for a given species actual leaf life spans vary widely among sites. From the above discussion a hypothesis can be formulated, which, like most hypotheses related to evolution, can be tested in the sense of fi nding 3.1 Norway Spruce or not a satisfactory historical narrative explana- tion rather than proving or falsifying a proposed In Norway spruce (Picea abies) silicon behaves causal law (see Mayr 1997, Chapter 4). as expected for a non-mobile element: its con- We hypothesize that in the absence of retranslo- centration increases between years linearly with cation of a particular nutrient, there is a deadlock, needle age, and within years much faster during because any improvement in the use of mobile the growing season than during the rest of the nutrients through longer leaf life-spans would year (Wyttenbach et al. 1991), suggesting that increase the immobilization of nutrients with low transpiration does not decrease much with needle mobility. Under strong selective pressure for long age. On the other hand, some decrease in tran- leaf life spans, a concurrent selective pressure spiration rate is expected to happen because of favouring boron redistribution should develop increased shading of ageing needles (e.g. Schoet- when this element’s availability is restricted (or tle and Fahey 1994), and because of restrictions high), which should have as a consequence that: to water fl ow by a more lignifi ed xylem (Ülo Species with very long-lived leaves are able to Niinemets, pers. comm.). redistribute B from old to young tissues. In this species, Finér (1989) observed a decrease in B concentration (r = –0.94, P = 0.002), and a steady increase in Ca concentration (r = 0.98, P < 0.001) with needle age (Fig. 1). This indicates 3 Evidence from the Forest that at this drained peatland site B was much more mobile in the trees than Ca. It was earlier postulated that B moved only in the Also in Norway spruce, Lehto and Mälkönen xylem, accompanying bulk water fl ow, accumu- (1994) studied the nutrient concentrations in the lating in old leaves (Dugger 1983). If this was true four youngest needle classes (older classes were for conifers, then B fl ow towards needles would also present but not sampled). They observed little be roughly proportional – discounting seasonal accumulation of boron with increasing needle age and year to year variation in soil availability – after the second winter, and a similar pattern for to the accumulated volume of water transpired, Ca (Fig. 2). This suggests redistribution of both B and over several years B concentration would and Ca, which does not agree with the data in Fig.
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