The Significance of the Accessory Tissues of the Hydrosystem For

IAWA Bulletin n.s., Vol. 5 (4), 1984 275

THE SIGNIFICANCE OF THE ACCESSORY TISSUES OF THE HYDROSYSTEM FOR OSMOTIC WATER SHIFTING AS THE SECOND PRINCIPLE OF WATER ASCENT, WlTH SOME THOUGHTS CONCERNING THE EVOLUTION OF TREES

H.l Braun Institut für Forstbotanik und Holzbiologie, Universität Freiburg, Bertoldstrasse 17, D-7800 Freiburg i. Br., F. R.G.

Summary The accessory tissues: Osmotic water shifting as a second principle of 1. The accessory tissues of the hydrosystem water ascent: consist of the parenchymatic contact tissue 7. The activity of the accessory tissues produces of the xylem rays, as weIl as the paratrachei a high osmotic pressure in the trees. This dal parenchyma in gymnosperms, and the brings about an uptake of water, often a po paratracheal contact-parenchyma in angio sitive pressure (system pressure ), and an os sperms. motic water shifting within the tree. 2. In the gymnosperms the accessory tissues are 8. The woody plants of the cool-temperate cli relatively poorly developed. In the xylem matic zones come into sap during the spring rays of tropical angiosperms the accessory time mobilisation phase as a result of this os tissues can be extensive and highly developed motic water uptake and water shifting. in the form of contact tissue of the xylem 9. In tropical deciduous trees it seems that os rays and of the paratracheal contact-paren motic water uptake and water shifting is - chyma. In the woody angiosperms of the in alternation with transpiration - a year temperate zone, however, the accessory tis round principle of water ascent. sues are in general only scantily present. 10. Some thoughts concerning the evolution of 3. The accessory tissues appear to be more ex pteridophyte, gymnosperm and angiosperm tensively developed in the roots than in the trees are discussed. shoot axes. Key words: Acid phosphatases, ecology, evolu Function of the accessory tissues: tion, osmotic water shifting, starch, water 4. The accessory tissues of tropical deciduous conduction, xylem parenchyma. trees are, in contrast to the rest of the paren chyma, always free of starch, and they con tinuaJly displayahigh activity of acid phos Introduction phatases. Deciduous trees 'come into sap' during the 5. The accessory tissues of deciduous trees in springtime mobilisation phase of the temperate the temperate zones store starch during the zone, which lasts from ab out the middle of winter, but in the spring this starch is broken March to the end of April, before the flushing down earlier than that of the rest of the pa of the leaves. Because there is still no transpira renchyma. This breakdown of starch marks tion stream, it has long been assumed that a the beginning of an intense activity of acid root pressure, presumably located in the endo phosphatases. This activity continues during dermis, was responsible for the water ascent in the springtime mobilisation phase (March, early spring. But there is no cJear evidence for April), then ceases suddenly with the flush a root pressure of this kind. According to Zieg ing of the leaves. The springtime activity of ler (1983) it can more probab1y be assumed acid phosphatases usually begins earlier in that 'coming into sap' is due to the release of the roots than in the trunk. The activity of osmotically active substances into the hydro the accessory tissues in the xylem is accom system, perhaps through living cells next to the panied by a breakdown of starch and an acti conducting elements of the xylem, which the vity of acid phosphatase in the secondary water must follow osmotically along a water phloem. potential gradient. This cou1d lead to a slow, 6. The activities of acid phosphatases in the ac unmeasurable water stream, a water shifting, cessory tissues only appear near water-con as Braun maintains on the basis of his investi ducting vessels which are fully functional. gations(1961a, 1980, 1982, 1983).

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There is, further, a second and related prob a) in gymnosperms, the paratracheidal parenchy lem. How do the quickly-growing woody plants ma in the tracheid ground-tissue and the paren of the hot, humid tropical lowlands er of the chymatous contact cells of the xylem rays. tropical and subtropical mountain forests cope b) in angiosperms, the paratracheal contact with the transport of water and nutrient salts parenchyma and the contact tissue of the under elimatic conditions permitting, at best, xylem rays (Braun, 1970, 1982, 1983). an impeded transpiration for only brief periods daily? Gymnosperms Haberlandt, as early as 1892, had already In gymnosperms the axial paratracheidal confronted this question. He determined that, wood parenchyma is generally only slightly de taken over longer periods of time and in com veloped. In the Pinaceae it is often completely parison with trees of the temperate zone, tran absent, as for example in the cases of Abies alba spiration is quite minimal under conditions of Mill., Picea abies (L.) Karst., Pinus sylvestris L.; very high relative humidity - which can reach or, as in the case of Larix, it is only scantily a saturation level of up to 99%; and in the rela present in single strands. In the Podocarpaceae, tively cool, always humid mountain forests it however, which are found primarily in the sub must be completely suspended for weeks at a tropical and tropical mountains of the southem time. But paradoxically, despite the minimal or hemisphere, it occurs more frequently. In Da nonexistent transpiration and despite the huge crydium and Podocarpus, in addition to the water supply of the soil, the leaves of many single strands short tangentially arranged rows tropical trees have structures which indicate a of parenchyma cells often occur between the protection against transpiration. These inelude, tracheids. Extensive pit contacts exist between according to Haberlandt, thick-walled epider these wood parenchyma cells and the tracheids, mises with heavy deposits of cutin, sunken thus characterising this parenchyma as a typical stomata - in shert, xeromorphic structures paratracheidal parenchyma (Fig. I). common to plants of drier locations or drier The parenchymatous cells ofthe gymnosperm elimates. Thus Haberlandt, contradicting Sachs, xylem rays always have elose pit contact to the who had described the 'transpiration stream' as axially arranged tracheids; these parenchymatic a condition sine qua non, recognised that green cells are thus contact cells, and the xylem rays land plants must have osmotic forces at their are contact rays (Braun, 1970). In a crossfield disposal which can generate a water supply there is either a large, simple, so-called fenestri from the roots to the crown of the highest tree, form pit, as for example in Pinus sylvestris and which are independent of transpiration and (Fig. I), or else 2 to 5 smaller, simple pits, as of a transpiration stream. for example in Abies alba. We will now attempt to elarify the questions thus raised. This shall be tried with reference to Woody angiosperms of tropical climates the microporous trees, which predominate in In the case of tropical woody plants, the pa the cool-temperate zone, and the macroporous ratracheal contact parenchyma can accompany woody plants, which are typical of the tropical the generally macroporous vessels in axially lowland (Acer- resp.Albizzia-organisation-fiIe of arranged single strands or as double or tripIe the hydrosystem after Braun, 1970); the warmth strands. It is much more common, however, requiring (thermophilous) cyeloporous woody that the paratracheal contact parenchyma sur plants of the Fraxinus-organisation-fiIe of the rounds one-quarter, one-third, one-half, three hydrosystem will be discussed later under the quarters, er all of the periphery of the vessels, same aspect. thus building either partial or complete sheaths around the vessels (Figs. 2 & 3; Braun, 1970). The contact tissue of the wood rays in tropi The accessory tissues cal woody plants with macroporous vessels is similarly extensive. When the radial course of Definition (Braun, 1983) a xylem ray touches a macroporous vessel, the Accessory tissues are parenchymatous tissues cells directly adjoining the vessels become con elosely linked with the special hydrosystem tact cells, Le., numerous pits, some of them (vessels and tracheids) by means of numerous quite large, connect these cells to the macro pits. Due to these elose pit contacts a functional paraus vessels. This contact differentiation of unity exists between the accessory tissues and the xylem rays is always present from the be the hydrosystem (Latin accessio = something ginning, and in tropical woody plants they are added). retained permanently, thus proving themselves Accessory tissues incIude the following: to be contact rays (Fig. 4; Braun, 1970).

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Fig. 1. The accessory tissues in gymnosperms, upper left: single paratracheidal parenchyma cells between the tracheid ground tissue of Larix decidua Mill.; upper right (dark cells), lower left (cells with starch): the paratracheidal parenchyma may be more extensively developed in (sub)tropical gymnosperrns (e.g. Podocarpus) than in gymnosperms of cooler climatic zones; lower right: paren chyma contact cells of the xylem rays, e.g. in Pinus sylvestris L., with large fenestriform pits to the tracheids (from Braun, 1970).

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HST

III",,.,,..-r-HST

.~I\--I!A\I~+-pKP

#f--iIP

Fig. 2. The accessory tissues in tropical deciduous trees; the paratracheaJ contact-parenchyma (pKP); partial sheaths of paratracheal contact-parenchyma in Tristania suaveolens Sw. (upper Jeft); more common, however, are 3/4 paratracheal sheaths or compJete paratracheaJ sheaths of para tracheal contact-parenchyma (upper right Saurauria bracteosa oe., lower left Albizzia procera Benth.). T = tracheids, ptdP = paratracheidal parenchyma, G = vessel, HST = xylem ray, ifP = inter fibrous parenchyma (from Braun, 1970).

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Fig. 3. Contact pits in the walls of macroporous vessels of tropical trees, leading to the paratracheal contact-parenchyma (lower left and upper right; from Gomes, 1985).

The tendency exists in tropical woody plants This tendency toward relatively slight devel to develop extensive accessory tissues - in the opment ofthe paratracheal contact-parenchyma form of paratracheal contact-parenchyma as - relative, that is, to that of the tropical woody contact tissue of the xylem rays. plants - can also be observed in the behaviour of the xylem rays. The secondary xylem rays in Woody angiosperms 01 the temperate zone trees of the temperate zone do always begin In woody plants of the temperate zone the with contact differentiation, i.e., all xylem ray paratracheal contact-parenchyma occurs along cells which touch avessei are connected to this the microporous vessels usually only in single vessel by numerous pits; but in the following or double strands (Fig. 5; Braun, 1970). Sheaths stage of xylem ray ontogeny, when the xylem of paratracheal contact-parenchyma, whether rays have become higher, the cells ofthe middle partial or complete, are entirely absent. cell rows are often forrned as isolation cells

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which, though also adjoining the vessels, pos Functional rhythm sess no pits to the vessels. Contact differentia The functional rhythm of the accessory tis tion in this case is restricted to the upper and sues may vary from one climatic zone to an lower parts of the rays (Fig. 6, Braun, 1970). other. Of the woody plants thus far investi In general, the accessory tissues of woody gated, in both the tropical and temperate zones, plants of the temperate zone are less extensive it may be said that: Iy formed than in the case of tropical trees. The accessory tissues in woody plants of the tropics are apparently always free of stareh. In roOfs Therefore these accessory tissues are character In the roots, particularly in shallow roots ised by a continuous activity of acid phospha which serve more for water conduction than tases, particularly at the contact pits. This is for anchorage, the vessels usually lie more most pronounced in the case of trees with con c10sely together than in the trunk. The larger tinuous or periodically intermittent growth. number of vessels in the roots occasions an in Only in the case of deciduous trees does this crease in the paratracheal contact-parenchyma. activity disappear, during and after the shedding In addition, the root vessels often have greater of leaves, and begins again with the growth of diameters than in the trunk. Thus an equivalent new shoots (Fig. 9; Fink, 1982). density of xylem rays will have more frequent The behaviour of the accessory tissues of contacts between the vessels and the xylem woody plants in the temperate climatic zones is rays. And the contact differentiation of the quite different. During the period ofwinter dor xylem rays to the vessels in the roots is also mancy starch can be stored in the accessory tis more extensively developed than in the trunk sues just as in other parenchyma. However, this (Fig. 7). starch will be the first to be broken down at the According to our investigations thus far it start of the springtime mobilisation phase. When can certainly be said that, in general, as far as the starch has been broken down, an intensive trees of the temperate zone are concemed, the activity of acid phosphatases begins in the acces accessory tissues in the roots are more exten sory tissues, above all at the contact pits (Figs. 10 sively developed than in the trunks. This ten & 11). This intensive occurrence of acid phos dency is also manifested in the fact that the phatases continues during the entire springtime contact pits of the xylem ray cells leading to mobilisation phase, which in Central Europe the vessels are often larger than in the trunk can occur in the period from the beginning of (Fig. 8). March to the middle of May. With the flushing of the leaves at the beginning of the growth pe The physiological activities of the accessory riod this activity of acid phosphatases in the ac tissues cessory tissues ceases as suddenly as it began. The springtime activity of acid phosphatases Physiological characteristics may begin in the roots as much as several days The accessory tissues, in contrast to other earlier than in the trunk (Fig. 11). wood parenchyma, do not store stareh. If they The high activity of acid phosphatases in the do store stareh, this starch is mobilised con accessory tissues during the mobilisation phase siderably earlier than that contained in the is, in addition, accompanied by an often very other parenchyma cells at the beginning of a sudden breakdown of the starch and the occur general mobilisation of stareh. rence of acid phosphatases in the secondary The accessory tissues may show a high activi phloem (Fig. 12; Sauter, 1966a & b; Braun, ty of acid phosphatases. This high activity of 1970, 1982, 1983). acid phosphatases is directly related to the car The activities of acid phosphatases in the ac bohydrate metabolism and to the active trans cessory tissues of trees of tropical and temper port of dissolved organic substances (e.g. Frey, ate zones occur only near functioning water 1954; Braun & Sauter, 1964a, b; Sauter, 1966a, conducting vessels. In the storage sapwood, in b; Sauter & Braun, 1968; Braun, 1970, 1983; which the rest of the parenchyma is still alive Fink, 1982). and full of starch, the accessory tissues of ves-

Fig. 4. The accessory tissues of tropical deciduous trees: the parenchymatic contact cells of the xylem rays. The cells of the xylem rays form numerous, and often large, contact pits to the vessels (above Terminalia superba Eng!. & Diels, radial), and do so in all stages of development of the xylem rays (I-phase contact rays; below Palaquium lobbianum Burck, tangential view). PZ = para tracheal contact-parenchyma, HF = wood fibres, G = vessel (from Braun, 1970).

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"'0 G

HF G HF G HF G

K ------. K-Differenzierung 1-phasig

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Fig. 5. The accessory tissues in woody plants of temperate c1imatic zones: the paratracheal contact parenchyma (pKP) often accompanies the vessels (G, FG) only in I or 2 strands (Ieft Fagus sylvatiea L., right Populus spee.). HST = xylem ray, ptdP = paratracheidal parenchyma, ifP = interfibrous parenchyma, JG = annual ring border (from Braun, 1970).

sels which no longer conduct water show no the mineral substances, potassium seems to be further activity of acid phosphatases. secreted primarily. These secretions of organic and inorganic substances can lead to a rise in Osmotic water shifting as a second principle of the pH-value of the vessel-water to 8 (Braun, water ascent 1980, 1982; Dimitri, 1967; Huber, 1960; Mar vin, 1958; Ziegler, 1983). Water uptake and water shilling in deciduous These substances secreted into the hydrosys trees 0/ the temperate zone during the mobili tem in early spring are osmotieally aetive. In sation phase be/are the flushing 0/ the leaves addition, there are large quantities of sugars in In trees of the temperate zone, in early spring the parenchyma of the secondary phloem which before the flushing of the leaves, organic and appear suddenly during the springtime mobili inorganic substances are secreted into the water sation of starch. Thus a high osmotie potential of the hydrosystem by the activity of the ac is produced in the roots and in the axial shoot cessory tissues. The greater part of the organic system of the tree in the early spring. substances are sugars (glucose, fructose, saccha As a result, the leafless trees take up water rose), which can compose as much as 97% of during this mobilisation phase. Using the hydro the dry matter. In addition, the water of the ponic system we have developed, which makes hydrosystem contains various organic acids, use of the growth container 06, it is possible to nitrogen compounds, vitamins and enzymes. Of (text eontinued on page 286)

Fig. 6. The accessory tissues in woody plants of temperate climatic zones: the parenchymatic contact cells of the xylem rays. In their young phase the xylem rays display contact differentiation to the vessels (KI). In the following phase of their development, however, the middle rows of cells of ten have no pit contacts anymore to the vessels (isolation differentiation; 2-phase contact-isolation rays; above Populus spee., radial; below Carpinus betulus L., tangential view). KOTÜ = contact pit, ISZ = isolation cell, Koz = contact cell, IZ = intercellular space, HF = wood fibre, FT = fibre tracheids (from Braun, 1970).

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G G G G

K------+ 2-phosig

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Fig. 7. The accessory tissues in roots. In the roots (right) the vessels usually lie more cIosely togeth er and have wider diameters than in the trunk (Jeft). This means that for an equivalent density of xylem rays there will be an increase in the contact tissue of the xylem rays and possibly an increase in the paratracheal contact-parenchyma (Fagus sylvatica L., x 40).

Fig. 8. In the roots (right) the contact cells of the xylem rays leading to the vessels usually have larger pits than in the trunk (left). (Quercus rabur L., radial).

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Fig. 9. Physiological behaviour of the accessory tissues of tropical trees. Above left: the accessory tissues (paratracheal contact-parenchyma and the contact cells of the xylem rays) are as a rule free of stareh, whereas the interfibrous parenchyma (dark) is very rieh in starch (Enterolobium cyclo carpum (Jacq.) Griseb.). Above right and lower left and right: high activity of acid phosphatases (black test precipitate) in the paratracheal contact-parenchyma, especially at the pits to the vessels, usually continuing yearround (above right Cordia colococca L., cross-section; below left Schizo lobium excelsum Vogel, radial; below right Cecropia peltata L., radial, from Fink, 1982).

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Fig. 10. Physiological behaviour of the accessory tissues in woody plants of the temperate climatic zones. In early spring the accessory tissues mobilise their starch earlier than the rest of the paren chyma. At the same time there begins an intensive activity of acid phosphatases (black test precipi tate), which then ceases after the springtime mobilisation phase with the flushing of the leaves. Left: high activity of acid phosphatases in the paratracheal contact-parenchyma and in the contact tissues of the xylem rays in Betula spec. Right: high activity of acid phosphatases in the contact cells of Populus xylem rays at the beginning of (above) and, especially at the cohtact pits, during (below) the mobilisation phase (right from Sauter, 1966b).

(text continued Irom page 282) Fraxinus) is higher than that of microporous measure exactly the water consumption of trees, e.g. Betula (Fig. 13). The daily water up woody plants plan ted therein, and to do so take during the mobilisation phase follows the continuously during any desired period (Braun, daily rhythm of the temperature, albeit with a 1983). Figure 13 shows the water uptake of certain delay: the strong increase of osmotic four tree species (8-10 years old, 4.5-5.5 m pressure in the tree during the midday hours high) during the mobilisation phase of 1982. due to the high activity of the accessory tissues The processes which lead to water uptake (acti makes itself feit in a forced water uptake only vity of the accessory tissues, sugar secretion into several hours later (Fig. 14). This water uptake the hydrosystem), as weil as the water uptake causes a gradual, but very large, increase in the itself, are dependent on the temperature, where water content of the tree's hydrosystem and in by the temperature threshold of the warmth the secondary phloem - rising from the roots loving ring-porous trees (Castanea, Quercus, into the shoot system (Braun, 1961 a).

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Fig. 11. Physiological behaviour of the accessory tissues in woody plants of the temperate climatic zones. The activity of acid phosphatases usually begins earlier in the roots (below, 18-3-71) than in the trunk (above), where it did not begin until 24-3-71. - . Fig. 12. The breakdown of starch and the activity of acid phosphatases in the accessory tissues of the xylem of trees in the temperate zones during the springtime mobilisation phases is accompanied by similar processes in the second ary phloem. Left, the secondary phloem still without any activity of acid phosphatases; right, two days later with a high activity (Acer pseudoplatanus L.; Braun, 1983).

Trees 'come into sap' in early spring as a re the cell walls of the feeder roots which take up sult of this osmotic water shifting (= water water. But this is prevented by the hydrophobie transport at a nonmeasurable rate (Gessner, Casparian strips in the anticlinal walls of the 1956). endodermis cells of the roots. This must cer Since this water uptake in leafless trees dur tainly be one of the essential functions of the ing the mobilisation phase is not relieved by any root endodermis (Ziegler, 1983). appreciable release of water, a positive pressure Woody plants of the temperate climatic zone develops in the hydrosystem (system pressure; come into sap during the springtime mobilisa Braun, 1983). It is this system pressure during tion phase before the [lushing of the leaves by the mobilisation phase which leads to the exu means of an osmotically conditioned water up dation of 'bleeding' sap if the xylem of a tree is take and water shifting. This principle ofwater injured. This sap is rich in organic and inorganic ascent is then rep/aced by the princip/e of tran substances (Ziegler, 1983). spiration du ring the phase of growth and depo The hydrosystem can only build up an excess sition (cf. Zimmermann, 1983). pressure if the solution under pressure is not But this is not always completely the case. able to escape downwards into the soil through For example. at the end of May 1983, when

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average week temperature Betula Castanea Quercus Fraxinus

12.-18.3.82 6.1 'e 70ml 19.-25.3.82 6.0 'e 100ml 26.3.-1.4. B2 8.9 'e 420ml BOml 2.- 8.4.82 12.1 'e 780ml 310ml t!83'~ 1370ml 9.-15.4.82 7.7 'e 3270 ml 970ml 50ml 340ml 096" 136Qml 16.- 22.4. 82 11.4 'C 15120ml 1600ml 405ml 930 ml .'00'(; 1.55 ml 23. 29.4.82 10.0 'C 21220m 2140ml 62Sml 1100ml i& 10 6"C 23-;,Jml 30.4.-6.5.82 10.4 'e 23620ml 2670ml 690ml 167Qm[

7. 13.5.82 11.8 'e 26 060 ml .4 660ml 1460ml 25BOmi

Fig. 13. Water uptake of trees (8-years old, 5-6 m tall) in the springtime mobilisation phase until the first opening of the buds. Note: the water uptake (and the activity of acid phosphatases) and therefore the mobilisation phase begins at a markedly higher temperature threshold in the ring porous, wannth-Ioving genera (Castanea, Quercus, Fraxinus) than in Betula (see also Braun, 1983).

the temperatures were low (8° C) and the hu also during the day in humid, overcast weather, midity very high, leaves of vines of the genus whenever as a result of high humidity and in Vitis secreted a sugary sticky sap. This also oc sufficient sunlight no transpiration takes place curs in Acer and other domestic tree species (Molisch, 1898; Figdor, 1898; Faber, 1915; during wann, humid periods ofsummer, though Fink, 1982). no hydathodes are present. Most probably un And so without doubt osmotic water shift der such conditions an osmotic water shifting ing must certainly be an essential principle of is set in motion by a revived activity of the ac transport in the uptake and provision ofwater cessory tissues, leading in the absence of tran and nutrient salts in tropical trees, one which spiration to a positive pressure in the hydro can function constantly, alternating with tran system and resulting in such a guttation. spiration, and in certain tropical regions may, over long periods of time, even be the dominant Water shifting in tropical deciduous trees as a principle of transport for water and nutrient year-round principle of water ascent, alterna salts. ting with transpiration This ecologically conditioned, continuous Whereas in deciduous trees of the temperate water shifting also becomes clearer if we con zone the activities in the accessory tissues sider that a xeromorphic leaf construction is around the vessels nonnally cease, the secretion very widespread among tropical trees (Haber of sugar into the vessels stop, and the positive landt, 1892; Richards, 1952; Walter, 1968). pressure in the hydrosystem disappears with According to Roth (1980), in humid tropical the onset of transpiration and the flushing of forests the leaves of tree species taller than the leaves; in the case of tropical trees there 1.30 m exhibit xeromorphic characteristics to may be a continuous activity of acid phospha an increasing degree, whereas in species of ta ses, even in a fully foliated state (Fink, 1982). sm aller statue, the leaves - especiaJly in the Presumably a high concentration of osmotical case of herbaceous plants - are hygromorphic Iy active substances is accumulated due to a (Roth, 1971, 1980, 1984). These scleromorphic steady secretion of sugars into the vessels, there leaves, along with the high humidity, impede by generating the conditions necessary for water transpiration still more. This renders osmotic uptake, water shifting and system pressure. And water shifting even more essential, and makes indeed, there is a bleeding pressure present in its pre-eminence in tropical trees even clearer. tropical trees, sometimes very high, mainly in An impeding of transpiration is perhaps physi the evening, at night and in the morning, but ologically necessary in order to avoid having to

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§ 'e 13.4.82 14.4.82 15.4.82 16.4.82,.., ,/ ", ! \. I \ \! ~

o o 12 o 12 o 12 o 12 o Fig. 14. Rhythm of the water uptake in the mobilisation phase before the unfolding of the leaves in Castanea sativa L. The water uptake increases with rising temperatures (air and trunk temperature); its daily peak (at night) occurs many hours later than the highest point of the temperature (midday).

convert too frequently from osmotic water tion, be it with passive, with active, or without shifting to transpiration, embracing as it does hydathodes. The guttation, which can be very the entire length of the hydrosystem and its intense, produces a watery solution of organic accessory tissues, from the roots to the tops of and inorganic substances (Ernst, 1876; Ziegler, the shoots. On the other hand, the xeromorphic 1983). Thus the positive pressure present in the leaves also prevent the take-up of water from entire hydrosystem due to the activity of the the air saturated with water vapour. A take-up accessory tissues, though unable to make itself of water through the leaves from the air could feit downwards through the roots due to the result in a diluting of the osmotic solution in barrier of the Casparian strips, can operate up the hydrosystem and lead to a complete water wards by means of the valve which guttation saturation of the leaves, which would be equal provides. And this determines as weil the direc Iy obstructive for osmotic water shifting and tion of an osmotic water shift. for transpiration. The scleromorphic leaves of Part of the osmotically active substances are tropical plants may therefore be an adaptation secreted by guttation. Nevertheless, including to humid climatic conditions and thus a defense the sugar produced during intensive assimila against water uptake from humid air. Perhaps tion, there may be on the whole a sugar surplus for this reason the term 'aerohygromorphic' which cannot be consumed or respired even (Greek: aer = air, hygr6s = moist, morphe = during very rapid growth. The surplus sugars form) is appropriate for this leaf construction, are apparently 'withdrawn from circulation' in which corresponds, at least partially, to xero the form of starch. This starch is stored in the morphic (Roth, 1980). Another fact prompting tissues of the interfibrous parenchyma and of osmotic water shifting is that the aerohygro the living wood fibres, both of which are fre morphic leaves are very often capable of gutta- quently quite extensive and often quite typical

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Thoughts conceming the evolution of trees, from an eco-physiological and anatomical point ofview It is presumed that the principles of osmotic water shifting and of transpiration suction were active from the very beginning. Possibly the principle of osmotic water provision has a tem poral advantage in evolution, since it also func tions in the parenchyma, and lower plants were and are largely dependent on parenchyma for water transport.

Pteridophyte trees The pteridophyte trees related to the Lepi dodendrales, Equisetales and Filicatae had their widest distribution during the Paleophytic peri od (Carboniferous, Lower Permian). The c1imate in this period was warm and very humid, i.e. , of a tropical character (Schwarz back, 1974), producing certainly only minimal transpiration stress. The secondary xylem, which in Lepidoden drales is only very slightly developed, was appa Fig. 15. In tropical trees the ground tissue of rently insignificant for water transport in these ten consists of living wood fibres which store trees (Bresinsky, 1983). Their linear leaves were starch and fat (thick-walled cells with dark con certainly mainly xeromorphic in structure, tents), in which large groups of interfibrous, which, insofar as it implied a reduction of starch-storing parenchyma cells are em bedded transpiration, was not an adaptation to the (thin-walled cells with dark contents) (Gledit warm-humid c1imate, but rather a protection sia lerox Desf. ; from Braun, 1970). against a water uptake from the very moist air ('aerohygromorphy', see above). It seems rea sonable to assurne that these pteridophyte trees effected the transport of water and nutrient salts mainly by means of the physiological prin for tropical trees (Fig. 15; Braun, 1970, Wol ciple of osmotic water shifting, primarily in the kinger, 1969, 1970, 1971; Fink, 1982). The parenchyma system of the bark, which was masses of starch in tropical trees are not re quite thick in these 'bark trees'. In the light of serves, but simply deposits of an osmotically this, the question as to the principle function inactive product of surplus sugar ('deposited of the ligule - whether primarily an organ of starch'). uptake or an organ of secretion - should prob Thus the following ecological/y conditioned ably be settled in favour of the latter alterna anatomical and physiological peculiarities are tive, Le. an organ of secretion' (guttation organ) characteristic of woody plants 01 warm-humid (Seyd, 1910; Liebig, 1931), This is supported or cool-humid tropics: by the evidence of the present-day quill worts I. Prominently developed accessory tissues (lsoetis species), which grow in the tropics ei which are continuously active. ther underwater or in moist soil; they need no 2. Osmotically conditioned water shifting with special additional structures for water uptake, positive pressure in the hydrosystem as a but they do require organs of guttation. main principle of water ascent along with transpiration. Gymnosperms 3. Xeromorphic leaves,. which may be inter At the beginning of the Mesophytic period preted as a protection against water uptake - in the Upper Permian - though the c1imate from the air ('aerohygromorphy') in order remained very warm, it became increasingly to maintain an osmotic water shift or, when arid. These are the preconditions for a high present, transpiration. transpiration stress. The pteridophyte trees 4. Capacity for intensive guttation. were not equal to this stress, having adapted 5. Large tissue groups of interfibrous parenchy themselves to a warm, humid c1imate by a ma and living wood fibres for the storage of prominent development of the principle of os 'deposited stareh'. motic water shifting, which permits only a very

Downloaded from Brill.com10/07/2021 04:48:33AM via free access IAWA Bulletin n.s., Vol. 5 (4),1984 291 slow movement of water. And so they largely a paratracheal contact parenchyma. Provided became extinct. with accessory tissues composed of the contact The age of gymnosperms began. They had the cells of the xylem rays and the paratracheal best prerequisites for withstanding the altered contact parenchyma, the angiosperms were also climatic conditions and the high demands on in the position to effectively manage their transpiration: a highly developed secondary transport of water and nu trient salts by means tracheid hydrosystem and xeromorphic leaves of an osmotic water shifting. Thus in the tropi for inhibiting transpiration. The accessory tis cal ecological conditions, where transpiration is sues - essentially present only as contact pa difficult, the angiosperm trees surpassed all renchyma of the xylem rays - could possibly other forms of vegetation in their ability to have produced a positive pressure in the hydro compete. And perhaps this accounts for their system following periods of cold weather. Such continued dominant role. a positive pressure would be in a position to If we consider in this connection the orga eliminate air embolisms which might have devel nisation 01 the hydrosystem 01 trees (Braun, oped after the thawing of the frozen water in the 1970, 1980, 1982) as represented by present hydrosystem. And perhaps this is also the rea day woody plants, one can imagine something son why our present conifers in high latitudes like the following (Fig. 16): The first angio and in high mountain regions are able to sur sperm trees had avessei hydrosystem with pa vive even long, hard periods of cold weather. ratracheal contact parenchyma as yet relatively incomplete. In the organisational scale of the Angiosperm trees hydrosystem this occupies the second level, af In the period which saw the development of ter that of the tracheid level of the gymno the angiosperms, the Cretaceous period, and sperms. At this level the vessels are still equip weil into the Paleocene, the climate became ped with relatively incomplete paratracheal warm and humid, tropical and subtropical contact-parenchyma and are embedded directly (Schwarzbach, 1974). On the basis of pollen in the tracheid ground tissue. Further, the organi analyses we may assurne that the early angio sation of the hydrosystem indicates a histologi sperms spread from the tropical zone of the cal differentiation, accompanied by a functional Lower Cretaceous to the north and south, division of labour, leading from the tracheid/ reaching in a relatively short time a dominant vessel level by way of a vessel/wood fibre level role under very uniform tropical conditions to avessellevel (Fig. 16). during the Middle Cretaceous (Ehrendorfer, The development of the paratracheal contact 1983). parenchyma, however, follows diverse paths. The advantage which the angiosperms attain They clearly indicate an adaptation within the ed under these conditions may have been de organisation al sequences of the hydrosystem to pendent on the development of avessei hydro the climate of particular climatic zones which system. This vessel system was accompanied by have gradually developed from the Tertiary on-

Fig. 16. Organisation of the hydrosystem of the trunk wood of trees (cf. Braun, 1970, 1982, 1983).- The organisation of the hydrosystem may be divided into a gymnosperm level (Ist level) and four angiosperm levels. Among the angiosperms one can recognise an ever-increasing histological differen tiation, accompanied by a functional division of labour, which progresses from the 2nd level, the tracheid/vessellevel ofthe hydrosystem, to a restricted tracheid/vessellevel (3rd level), a vessel/wood fibre level (4th level), and culminating in a vessel level of the hydro system (5th level). One can also recognise three organisational sequences in the organisation of the hydrosystem: a macroporous Albizzia odoratissima sequence, typical of tropical trees, a ring-porous Fraxinus excel sior sequence of warmth-loving, Mediterranean woody plants, and an Acer pseudoplatanus sequence of woody plants of cool-temperate climatic zones. The paratracheal contact-parenchyma, as apart of the accessory tissues, is diversely developed in these organisational sequences: in the 2nd organisationallevel (at the lower stage of the sequences) the paratracheal contact-parenchyma is still relatively scantily developed in all the sequences. In the tropical Albizzia sequence the paratracheal contact-parenchyma continually increases through the 3rd and 4th levels to complete sheaths in the Albizzia type of the highest (5th) level. The same is true of the macroporous earlywood vessels ofthe Fraxinus sequence. However, among the structural types of the Acer sequence, the trees of the temperate climatic zones, the paratracheal contact parenchyma is relatively scantily developed in all the levels (cf. text).

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Downloaded from Brill.com10/07/2021 04:48:33AM via free access IAWA Bulletin n.s., Vol. 5 (4),1984 293 ward. This adaptation of the vessel system with Bresinsky, A. 1983. Pteridophyta. Lehrbuch der its paratracheal parenchyma is manifested in Botanik. 32. Aufl. G. Fischer, Stuttgart, three organisational sequences, two of which New York. may be singled out (Fig. 16). The Albizzia se Dimitri, L. 1967. Untersuchungen über die Ätio quence is characteristic of the tropics with a logie des 'Rindensterbens' der Buche. Forst warm or hot, humid c1imate. Here we find, wiss. Centralbl. 86: 257-276. from the simplest to the highest forms, an ever Ehrendorfer, F. 1983. Evolution und Systema more pronounced development of the para tik. Lehrbuch der Botanik. 32. Aufl. G. tracheal contact parenchyma, culminating in Fischer, Stuttgart, New York. the complete sheaths of the most highly devel Ernst, A. 1876. Botanische Miscellaneen. 3. oped type of this sequence, the Albizzia odora Tropfenausscheidung bei Calliandra saman. tissima type. We find further: osmotic water Bot. Zeit. 34: 35-36. shifting, along with transpiration, as a main Faber, F. C. 1915. Physiologische Fragmente aus principle of water and mineral transport (fre einem tropischen Urwald. Jahrb. wiss. Bot. quent positive pressure in the vessel system, 56: 197-220. high capacity for guttation); large groups of in Figdor, W. 1898. Untersuchungen über die Er terfibrous parenchyma for the absorption of scheinung des Blutungsdruckes in den Tro deposited starch; xeromorphic (aerohygromor pen. Sitzungsber. math.-naturw. Cl. Kaiserl. phic) leaf structure; animal pollination and Akad. Wiss. Wien C VII, Abt. I. conspicuous hermaphroditic flowers, as must Fink, S. 1982. Histochemische Untersuchungen have been the case from the very beginning of über Stärkeverteilung und Phosphataseakti the angiosperm period, since wind pollination vität im Holz einiger tropischer Baumarten. is and was impossible under conditions of high Holzforschung 36: 295-302. air humidity. Frey, G. 1954. Aktivität und Lokalisation von The Acer sequence is characteristic of tem saurer Phosphatase in den vegetativen Teilen perate c1imates (also in the high mountain trop einiger Angiospermen und in einigen Samen. ics). Here we find a constant, relatively weak de Ber. Schweiz. Bot. Ges. 64: 390-452. velopment ofthe paratracheal contact-parenchy Gessner, F. 1956. Wasserspeicherung und Was ma; osmotic water shifting only during the mo serverschiebung. Handb. Pflanzenphysiol. 3: bilisation phase, transpiration during the growth 247-256. and deposition phase; mesomorphic leaf struc Gomes, A. V. 1985. Functional histology of the ture;-and a strong tendency toward wind pol wood Sc1erocarya caffra Sond. (Anacardia lination and inconspicuous unisexual flowers. ceae). IAWA Bull. 6: in preparation. Haberlandt, G. 1892. Anatomisch-physiologi References sche Untersuchungen über das tropische Braun, H.J. 1961a. Die frühjahrszeitliche Was Laubblatt. Sitzungsber. Kaiserl. Akad. Wiss. serverschiebung in Bäumen und Pfropf Wien, Math.-naturwiss. Classe 101: 785- reisern. Zeitschr. f. Bot. 49: 96-109. 816. - 1961 b. The organisation of the hydrosys Huber, B. 1960. Die Gewinnung von Ahorn tem in the stemwood of trees and shrubs. zucker in Kanada. Allgern. Forstzeitschr. IAWA Bull. 1961/2: 2-9. 15: 291-292. - 1970. Funktionelle Histologie der sekundä• Liebig, H. 1931. Über die Funktion der Ligula aren Sprossachse. 1. Das Holz. Handbuch der von Isoetes lacustre. Flora 126: 111-114. Pflanzenanatomie (Encyc1opedia of Plant Marvin, J.W. 1958. The physiology of Maple Anatomy). Borntraeger, Berlin, Stuttgart. sapflow. In: Physiology of forest trees - 1980. Bau und Leben der Bäume. Rombach, (K. V. Thiemann, ed.), New York. Freiburg i. Brsg. Molisch, H. 1898. Über das Bluten tropischer - 1982. Lehrbuch der Forstbotanik. Fischer, Holzgewächse im Zustand völliger Belau Stuttgart, New York. bung. Ann. Jard. Bot. Buitenzorg 2, Suppl.: - 1983. Zur Dynamik des Wassertransportes in 23-32. Bäumen. Ber. Deutsch. Bot. Ges. 96: 29-47. Richards, P. W. 1952. The tropical rain forest. - & J. J. Sau ter. I 964a. Phosphatase-Lokalisa Cambridge Univ. Press. tion in Phloembeckenzellen und Siebröhren Roth, 1. 1971. Morphological and anatomical der Dioscoreaceae und ihre mögliche Be studies of leaves of the plants of a Venezue deutung für den aktiven Assimilattransport. lan c10ud forest. 1. Shape and size of the Plan ta 60: 543-557. leaves. Acta Biol. Venez. 7: 127-155. - & - I 964b. Phosphatase-Aktivität in den - 1980. Blattstruktur von Pflanzen aus feuch Siebzellen der Koniferennadeln. Naturwis ten Tropenwäldern. Bot. J ahrb. Syst. 101: senschaften 51: 170. 489-525.

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- 1984. Stratification of tropical forests as Schwarzbach, M. 1974. Das Klima der Vorzeit. seen in leaf structure. Nijhoff / Junk, The 3. Aufl. F. Enke, Stuttgart. Hague. Seyd, W. 1910. Zur Biologie von Selaginella. Sauter, J.J. 1966a. Untersuchungen zur Phy Diss. Phil., Fakultät Univ. Jena. siologie der Pappelholzstrahlen. I. J ahres Walter, H. 1968. Die Vegetation der Erde in öko• periodischer Verlauf der Stärke speicherung physiologischer Betrachtung. I. Die tropi im Holzstrahlparenchym. Zeitschr. Pflan schen und subtropischen Zonen. Fischer, zenphys. 55: 246-258. Jena. - 1966b. Untersuchungen zur Physiologie der Wolkinger, F. 1969, 1970, 1971. Morphologie Pappelholzstrahlen. 11. Jahresperiodische und systematische Verbreitung der lebenden Änderungen der Phosphatase-Aktivität im Holzfasern bei Sträuchern und Bäumen. I. Holzstrahlparenchym und ihre mögliche Zur Morphologie und Zytologie. Holzfor Bedeutung für den Kohlenhydratstoffwech schung 23: 135-144. 11. Zur Histologie. sel und den aktiven Assimilattransport. Holzforschung 24: 141-151. III. Systemati Zeitschr. Pflanzenphys. 55: 349-362. sche Verbreitung. Holzforschung 25: 29-30. - & H. J. Braun. 1968. Histologische und zy Ziegler, H. 1983. Physiologie. Lehrbuch der Bo tochemische Untersuchungen zur Funktion tanik. 32. Aufl. G. Fischer, Stuttgart, New der Baststrahlen von Larix decidua MiII., York. unter besonderer Berücksichtigung der Zimmermann, M.H. 1983. Xylem structure and Strasburger-Zellen. Zeitschr. Pflanzenphys. the ascent of sap. Springer, Berlin, Heidel 59: 420-438. berg, New York, Tokyo.

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