Carlos López Ocaña
Ph.D., M. of Sc., Agronomist
Principal Prof. Dept. of Biology, Director of CIZA
National Agricultural University
Prosopis tamarugo Phil. is a leguminous tree 10 to 20 m tall, endemic to the Chilean northern desert, located beyond the Coastal Mountain Range. In this area, tamarugo forms a vast forest at some 1,000 m altitude, on a totally flat land known as Tamarugal Pampa, partly buried under a salt crust. This is the only place in the world where mature tamarugo occurs.
Like other species of the genus Prosopis, tamarugo not only produces wood, but also fodder for livestock. Tamarugo fruit and leaves have been successfully used for many years as fodder for sheep and goats, with an animal stocking rate of approximately 4 sheep per ha, thanks to the quality of the legumes which contain around 5% crude protein and 55% total digestible nutrients (Kammalade & Kammalade Jr. 1965, in Cadahia 1970). Its fruit and leaf yield is significant, varying from 4,000 kg/ha in 10-year-old plantations to nearly 15,000 kg/ha in 35-year-old plantations (Cadahia 1970). The wood has been used extensively; however, very little is known about its properties.
Besides the assets mentioned above, tamarugo has very outstanding water requirement peculiarities, as it needs irrigation only during the first half-year of its life (every 4 or 5 days at the nursery and every 10–20 days after transplanting in the field).
Once it has established itself in the desert, it grows very quickly without irrigation, reaching a height of 2 to 2.5 m in 3 to 5 years (Botti & Sudzuki 1970). The establishment rates are 80% to 90% at the end of the first year (Carvallo 1970). Furthermore, tamarugo thrives on soils with a saline crust ranging in thickness from 0.10 m to 0.40 m over a sandy subsoil, and in places where the groundwater table lies so deep, that its roots—which penetrate as deep as 7 to 8 m— cannot reach it (Toro 1967; Sudzuki 1969).
Considering that little knowledge is available on the growth and development of this exceptional species, a trial was designed under controlled environmental conditions to study the effect of various thermoperiods on its growth and transpiration during the first year after germination. This paper deals exclusively with the studies on growth.
2. METHODS AND MATERIALS
Prosopis tamarugo Phil. seeds, previously treated with sulphuric acid, were made to germinate in vermiculite, in pots 8 cm in diameter.
The effect of 8 different thermoperiods (treatments) on the growth was studied, in air-conditioned greenhouses at the Laboratory of Desert Biology of the University of Reno, Nevada, USA, from November 1971 to December 1972. Ten 1-month-old seedlings were used per treatment.
One of the greenhouses was kept at 20° C during the day and 10° C during the night, and the other one at 30° C during the day and 20° C during the night.
A photoperiod of 16 hours of light and 8 h of darkness was used in all the treatments. Day-light was complemented at the greenhouses with fluorescent lamps 100 candle-foot in intensity to complete the 16-hour daylight period. An air-conditioned laboratory, equipped with fluorescent lamps 200 candle-foot in intensity was kept at 10° C during the day and 5° C during the night. The central area of the phytotron was maintained at 17° C.
In each treatment, the plants were placed in movable, adjustable iron structures, moved daily at 8 h and 18 h, according to the thermoperiod.
All the plants were irrigated daily with Hoagland complete nutritive solution, slightly modified (Went, 1957).
The treatments were as follows:
Day 10° C - Night 20° C (D10-N20)
Day 20° C - Night 5° C (D20-N 5)
Day 20° C - Night 10° C (D20-N10)
Day 20° C - Night 20° C (D20-N20)
Day 30° C - Night 5° C (D30-N 5)
Day 30° C - Night 10° C (D30-N10)
Day 30° C - Night 17° C (D30-N17)
Day 30° C - Night 20° C (D30-N20)
From the 16th to the 18th week after the initiation of the treatments, the thermoperiod was temporarily changed for a group of plants in 6 of the treatments, measuring the length of the stem daily. The temperature changes are shown in bold face:
From D20 — N 5 to D30 — N 5
From D20 — N10 to D20 — N20
From D30 — N 5 to D30 — N17
From D30 — N17 to D30 — N 5
From D30 — N20 to D20 — N20
From D20 — N20 to D20 — N10
2.2 Growth Measurements
All the plants were left with only one stem. The length of the stem and the number of leaves were measured weekly. The dry weight of the leaves, stems and roots was also determined. As the the plants developed, the guides and metal supports were graduated accordingly in order to avoid intertwining of stems, making measure taking easier to perform and insuring uniform illumination.
2.3 Transpiration Measurements
Transpiration was measured in three periods of 24 hours each, two in summer and one late in the fall, using the transpirometer method developed by Went (1957) and Stark (1967). Three plants were used per treatment.
3.1 Initial Treatments
Figure 1 illustrates the growth measurements for 6-week periods. Figure 2 shows the height of the tamarugo plants at the end of the 16th and 31st week. The plants under the thermoperiod D30- N20 showed the greatest growth rate in the first 25 weeks, followed by treatments D30 - N17, D20 - N20, D30 - N5, D20 - N10 and D20 - N5, in that order.
After the 80th week, stem measuring was discontinued, first of treatment D30 - N20 and, at the end of the 37th week of the treatments, D30 - N17, D20 - N20, D30 - N10 and D30 - N5. Since the plants in treatments D20 - N10 and D20 - N5 continued increasing their growth rate, measurements were continued until the 55th week, when the growth rate dropped dramatically. T-Tests were applied between growth regression coefficients for a selected number of weeks in the various treatments. A significant difference was found between treatments D30 - N20 and D30 - N17 up to the 28th week; thereafter, there was a marked drop in the former's growth rate, due to the size of the pot. There was no significant difference between treatments D30 - N17 and D20 - N20. The difference in growth among the remaining treatments was highly significant. The greater the day and night temperatures, the greater the growth rate.
3.2 Temporary Change of Thermoperiods
Figure 3 summarizes the effect of the temporary change —from the 16th to the 18th week — both of the phototemperature and the night temperature on the growth of the plants in 6 of the treatments.
The temperature changes are shown in bold face. In all of the cases there was an increase in the growth rate when the temperature was increased, either during the day or the night, and vice-versa. Both the plants in treatment D30 - N5 and in D20 - N10 enlarged their leaves when they were changed to D30 - N17 and D20 - N20, respectively (Fig. 4).
The plants in treatment D30 - N5 showed anthocyanin in the stems and thorns when they were changed to D20 - N5.
After the plants had been returned to their original treatments, it was observed that the temporary changes mentioned above produced a post-effect (in the same direction) on the growth rate, for about two weeks.
3.3 Continuation of the Initial Treatments
The number of leaves in every plant was counted weekly in the various treatments during the first five weeks, and every 2 weeks from the 6th to the 23rd week. The increase in the number of leaves was higher with higher day or night temperature. The plants in treatment D20 - N10 and D20 - N5 increased their production of leaves after the 23rd week, to drop dramatically after the 47th week. According to Test - T taken among the regression coefficients of leaves per plant for the various treatments, there was no significant difference between D30 - N20 and D30 - N17.
The shoot/root ratio on dry weight basis was also greater as the day or night temperature increased (Fig. 5).
In treatment D30 - N17, the plants showed a smaller shoot/root ratio than those under D30 - N20, due to the greater growth of the root system in the second treatment.
Figure 6 shows clearly that the growth of stem and leaves, expressed as dry weight, also increases when the temperature increases. A striking feature was the production of 4-pinnate leaves (the species is normally bi-pinnate) in the treatments with 30° C phototemperature and in D20 - N20, with greater number of leaves per plant when the night temperature increased. Foliole number was smaller in plants from the treatments D20 - N5 (7 to 10 pairs) than in those with 30° C day temperature (12 to 13 pairs).
3.4 Transpiration Measurements
The variance analysis indicated a highly significant difference in favor of the summertime transpiration rates compared with those of the fall. There was no significant difference among the treatments. The transpiration rate of tamarugo in no case exceeded 1 × 10-4 water/cm2/min.
4.1 Initial Treatments
The comparison of plant growth in the various treatments shows dramatic differences, particularly under the low sunlight conditions of the winter season. In this season the growth rate of the tamarugo plants was greatly influenced both by daytime and nighttime temperature; even more, the combination of cool days (20° C) with cold nights (5 to 10° C) stopped their growth.
With the intense sunglight of the summer of 1972, the growth rate of tamarugo increased in all the treatments, being particularly outstanding in D20 - N5 and D20 - N10.
The highest height gain of tamarugo was 122 mm/week in thermoperiod D30 - N20, far above the greatest height gain shown by Prosopis juliflora (SW) DC (90 mm/week) in a parallel trial.
Analyzing the growth rates shown in Fig. 1, it can be seen that in all treatments the increases were maintained until the 24th–28th week. At that time the plants in treatment D30 - N20 measured 2 m. After that size, the growth rate dropped as a result of the small size of the pots and the consequent water problem.
The height gains of tamarugo in treatment D30 - N5 were remarkably good, evidencing the great flexibility of this species to adjust rapidly its metabolic profiles to such extreme thermoperiods as 25° C every 12 hours.
According to Went, 1957, the optimum thermoperiod for most species is that which has a difference of 3° to 7° C between the minimum and the maximum; for tamarugo this difference was 10° C, and it attained excellent growth even with a difference of 25° C.
Shortly after the trial was started, the plants in treatments with 5° C night temperature became anthocyanic at the terminal shoots and stipular thorns. It is an established fact that the anthocyanin synthesis is influenced by changes from high to low temperatures (Martin et al. 1972) and by long photoperiods (Went 1957). It was subsequently found that sunlight also influences this process in tamarugo. Indeed, the anthocyanin disappeared first from the plants in D30 - N5 and later in those plants in D20 - N5 parallel to the increase in sunlight in late spring and early summer, a fact which showed that intense sunlight (i.e., above 400 g-cal/cm2/day) had neutralized the effect of the long photoperiod-low night temperature interaction.
Another interesting observation was the temporary withering of the tips of the shoots during the first eight weeks in plants under treatments of 5° C during the night. The low night temperature apparently had an influence on the water uptake of the still small root system, being transpiration higher than absorption (Kozlowski 1964). This effect was neutralized experimentally by rising the temperature to 10° C around the pot. Subsequently, when the roots had attained sufficient development, withering disappeared.
4.2 Effect of the Temporary Change in Thermoperiod
Figure 3 shows clearly that the plants most severely affected were those changed from D20 - N10 to D20 - N20 and from D20 - N20 to D20 - N10.
These findings corroborated a fact that was evident just by looking at the plants in the original treatments D20 - N10 and D20 - N20; i.e., that a difference of 10° C in the night temperature was critical for tamarugo growth when it was combined with cool days (20° C). The dramatic difference between both treatments seems to be a result of the greater translocation of sugar in nights with high temperature (20° C) followed by cool days. An indication thereof was the marked preference of Aphides for the growth tips of tender leaves early in the morning in treatment D20 - N20.
The findings of the phototemperature change in D30 - N5 to D20 - N5 corroborated the effect of the low phototemperature on the anthocyanin synthesis. In fact, the upper portions of the shoots turned reddish during the two weeks in which daytime temperature was kept at 20° C.
4.3 Continuation of the Initial Treatments
During the spring of 1972 substantial changes were observed in the growth of the tamarugo plants in treatments D20 - N5 and D20 - N10, which increased their growth rates 7 and 5 times, respectively, in comparison to the winter months. This reveals a remarkable increase in the net photosynthesis during the spring months, which has a daily sunlight average of over 550 g-cal/cm2.
A morphogenetic effect of the thermoperiod, accentuated by the increased sunlight, was the production of 4-pinnate leaves in all the plants grown under phototemperature of 30° C and in those of D20 - N20. The greater the daytime and nighttime temperature, the greater the size of the plants and the number of 4-pinnate leaves produced by the plant. The formation of this type of leaves precisely by the large plants was probably a consequence of the great vigour determined by the optimum environmental conditions. The leaves in treatments D20 - N 5 and D20 - N10 were always bipinnate, even during their best growth period.
As expected, the dry weight of leaves, stems and roots increased parallel to the increase in daytime and nighttime temperatures. The case was the same for the shoot/root ratio. A similar effect of temperature on the root system was observed by Cochrane in peppers and by Went in tomatoes (Went 1945).
Treatments D20 - N5 and D20 - N10 were the only ones which continued beyod the 37th week, reaching the 55th week. In these treatments the plants attained the highest growth rates in the fall, when sunlight was well below 400 g-cal/cm2/day. Later on, in the winter of 1972, these plants slowed the rhythm of their growth drastically, to a minimum that was similar to that attained the previous winter (Fig. 1). In this case, the limiting factor was apparently the sunlight.
4.4 Transpiration Measurements
Preliminary results of the transpiration measurements indicated that the direct effect of sunlight on tamarugo transpiration and the duration of its after-effects depend on the amount of short wave energy which the plants can absorb during the day. The greater the sunlight, the stronger seems to be its immediate and after-effect, and less clear the influence of the thermoperiod in transpiration. The after-effect of sunlight decreases markedly during the night. The controlling effect of the thermoperiod on the transpiration in clearer under conditions of low sunlight.
The fact that the transpiration rates obtained under controlled conditions agree with those determined in the natural environment of tamarugo is quite relevant. The values obtained for each case were far below 1 × 10-4 water/cm2/minute, evidencing a strong resistance to transpiration.
5.1 Under conditions of low sunlight (i.e. below 300 g-cal/cm2/day), the growth of tamarugo is so strongly influenced by the thermoperiod that, on the one hand, the combination of cool days and cold nights (D20 - N5) stops its growth almost completely and, on the other hand, the combination of warm days and warm nights (D30 - N20) induces high growth rates.
5.2 Intense sunlight (i.e. above 400 g-cal/cm2/day) increases the growth of tamarugo; even in treatment D20 - N5, growth increased considerably. Its after-effect is also strong.
5.3 Prosopis tamarugo shows a relatively fast growth rate even under extreme thermoperiods, such as D30 - N5, which evidences the great flexibility of this species to rapidly adjust its metabolic processes to a rhythmic fluctuation of 25° C every 12 hours.
5.4 When the daytime or the nighttime temperature is increased temporarily, the growth rate of tamarugo increases, and vice-versa.
5.5 Other growth expressions, such as the number of leaves per plant, dry weight of the leaves, stems and roots, shoot/root ratio and measurements of total length of stems after a pruning, also indicate that tamarugo grows faster with higher daytime or nighttime temperatures.
5.6 The anthocyanin synthesis in stems and thorns of tamarugo is induced by the interaction of low sunlight during the day and cold nights (5° C) or by the sharp decrease in phototemperature with cold nights. The intense sunlight not only neutralizes the systhesis of the pigment, but also determines its reabsorption. The reabsorption and blocking of the synthesis of the pigment are faster in warm days (30° C) than in cool days (20° C).
5.7 During the first months of their life, the seedlings undergo a temporary withering when subjected to low night temperatures (5° C).
5.8 The interaction of high daytime and nighttime temperatures and intense sunlight has a morphogenetic effect on tamarugo; it produces 4-pinnate leaves instead of the normal bipinnate ones when the phototemperature is 30° C, and also when the thermoperiod is D20 - N20. The greater the daytime and nighttime temperature, the greater is the number of 4-pinnate leaves produced by each plant.
5.9 The preliminary findings indicate low transpiration rates in tamarugo.
5.10 The optimum environmental conditions for the growth of tamarugo found in this trial coincide with those occurring at its place of origin.
BOTTI C., SUDZUKI F. 1970 Relaciones hídricas del tamarugo Prosopis tamarugo Phil., en la localidad de Canchones. Universidad de Chile. Santiago, Chile.
CADAHIA D. 1970. Informe sobre el plan forestal ganadero Pampa Del Tamarugal, Depto. de Tarapacá. Corporación de Fomento de la Producción. Estudio elaborado para el BID, Santiago, Chile.
CARVALLO N. 1970. Determinación de tasas de riego en la plantación de Prosopis tamarugo Phil. Thesis for Forest. Eng. Deg., Universidad de Chile, Santiago, Chile.
KOZLOWSKI T.T. 1964. Water metabolism in plants. Harper and Row Publishers, New York.
MARTIN C.L., PAYNOT & J.C. VALEE. Quelques effets de la temperature sur la floraison, le metabolisme aminé et l'anthocyanogénese, phytotronique et prospective horticole. 18 Congres International de L'Horticulture. Gauthier - Villars Editeur. Paris.
STARK N. 1967 The transpirometer for measuring the transpiration of desert plants. Journal of Hydrology 5: 143–157.
SUDZUKI F. 1969 Absorción de agua atmosférica en tamarugo (Prosopis tamarugo Phil.) I. Observaciones sobre riego foliar en plántulas de tamarugo. II. Aplicación foliar de THO en plántulas de tamarugo. III. Absorción foliar de agua atmosférica en tamarugo. Universidad de Chile. Est. Exp. Agron. Bol. Téc. 3-: 1–23, Santiago, Chile.
TORO J.M. 1967. Desarrollo radicular del tamarugo. Informe Interno. Fac. de Agronomía de la Universidad de Chile, Chile.
WENT F.W. 1945. Plant growth under controlled conditions V. The relation between age, light, variety and thermo-periodicity of tomatoes. Am.J. Bot. 32 (8) : 469–479.
WENT F.W. 1957. Experimental Control of Plant Growth. Vol. 17. Chronica Botanica Co., Waltham, Mass.
Fig. 1. Growth rates (mm/week) of Prosopis tamarugo under different thermoperiods, for successive 6-week periods (Nov. 14 1971–Dec. 9 1972).
Fig. 2. Prosopis tamarugo under the various thermoperiods. Top: 16th week. Bottom: 31st week. From left to right: plants in treatments D20-N5, D20-N10, D20-N20, D30-N5, D30-N10, D30-N17 and D30-N20.
Fig. 3. Effect of the temporary change in thermoperiod (15 days) on the growth of Prosopis tamarugo. The temperature changes are shown in bold lettering.
Fig. 4. Tamarugo plant from treatment D20-N10.
Left: large leaves provoked by the change of night temperature to 20° C (effect of the temperature). Right: the same plant 10 weeks later; the large leaves in the mid portion of the stem are the same as in the plant on the left, and the large leaves of the upper portion have resulted from the effect of the increase in sunlight during the spring (effect of sunlight).
Fig. 5. Shoot/root ratio, on dry weight basis, of tamarugo plants 9 months old growing under various thermoperiods.
Fig. 6. Dry weight of leaves and stem of 9-month-old tamarugo plants growing under various thermoperiods.
University of Chile
All living organisms must adapt to the environment in order to survive and reproduce. Natural selection, the inexorable driving force behind this adaptation, provides the organisms with an enormous variety of abilities, enabling them to make use of the available resources. Each organism, therefore, ought to be regarded as a microcosmos immersed in a vast ecosystem and, for a good encompassing view, we must understand its parts, i.e., the individual.
The ability of a plant to thrive in a xerophytic environment is linked to its capacity for developing a suitable root system and foliar morphology to enable it to carry out its biologic processes adequately. Plants regulate their correlation with the environment through their own internal mechanisms, which control the extent and kind of modifications necessary to adapt to the prevailing conditions thereof.
According to Etherington (1978), the capacity for survival of a given plant is closely related to its greater or lesser capacity for undergoing strategic changes. A common example, found at practically every environment, is the rapid change —even in fractions of a second— of the respiratory and photosynthetic rate.
Several authors (Cunningham & Strain 1969; Smith & Nobel 1977a, 1977b and 1978; Ehleringer et al. 1976) have discussed the seasonal changes in the morphology of the leaves of perennial desert shrubs and analyzed their relations with temperature, dry seasons in the year, effects of radiation, soil moisture and leaf temperature, finding various morphological and climatological correlations.
The purpose of this work is solely to provide evidence for some morphological changes which tamarugo folioles undergo when growing in different environments, and intends to make a description of the observations without analyzing the causes, as the variability of the material demands a more thorough and methodical study.
MATERIALS AND METHODS
Leaf samples used in the research study were obtained from trees growing at 14 different sites in the Tamarugal Pampa (69° 35'W and 20° 30'S at 1,200 m above sea level [asl]), with varying soils and groundwater table depths. Additionally, material from San Pedro de Atacama (68° 20'W and 22° 55'S at 2,436 m asl), Caldera (70° 50'W and 27° 5'S at 10 m asl) and Santiago (70° 40'W and 33° 30'S at 520 m asl) was also included. Foliole anatomy was compared for seedlings grown at Canchones (Tamarugal Pampa) and in a greenhouse in Santiago. The observations were made on green material and permanent preparations.
FAA was used as fixer. The material was dehydrated with ethyl alcohol series and enclosed in paraffin (Johansen 1940). The slices of green and fixed material were dyed with various dyestuffs and combinations thereof (Johansen 1940), from which Safranin-picro-aniline blue was selected for use.
Observations were made with a Nikon Labophot contrast phase optical microscope.
Even though tamarugo types have not been taxonomically differentiated, two growth habits can be observed at the Tamarugal Pampa: one in which the canopy is made up of straight rigid branches, and another one in which the branches tend to droop. The first one is normally less fruitful than the latter. Foliole samples were collected separately from each growth type, dubbed Fastigiate and Drooping, respectively.
Table 1 presents details of the type of material used.
DESCRIPTION OF THE MATERIAL
Figure 1 shows a schematic summary of the typical structure of a tamarugo leaf adult foliole.
Figure 1. Scheme of a tamarugo leaf foliole crosscut. The indicated figures correspond to the maximums and minimums recorded. A. Adaxial face stoma; a. special cells (S.C.), b. bundle sheath with the cells which acquire the same hue as the S.C. with the dyestuffs used. B. Abaxial epidermis.
The paripinnate folioles —6 to 12 pairs— of the tamarugo leaves are glabrous, elyptic-oblong, 3–6 mm in length and 1–2 mm wide, apex obstuse or slightly apiculate.
Provenance of the samples analyzed, indicating relevant soil characteristics, type of tree and sampling date.
|Location||Characteristics||Type of tree||Date|
|Quillagua||Moist soil near Loa River, very brackish||Fastigiate||21-XII-68|
|Barreda||5-cm salt crust||Fastigiate||29-XII-68|
|Barreda||Water table at 8 m||Drooping||29-XII-68|
|5-cm salt crust. Water table at 8–10 m||Drooping||29-XII-68|
|Sulfatera||Highly saline water near surface||Fastigiate||28-XII-68|
|Junoy||20-cm salt crust||Fastigiate||19-I-68|
|Water table at 14 m||Drooping||19-I-68|
|Sta. Emilia||Sand without salt crust||Fastigiate||18-VII-69|
|Canchones||Sand without salt crust||Fastigiate||22-XI-68|
|Water table at 12 m||Drooping||22-XI-68|
|Gatica||40-cm salt crust||Fastigiate||24-I-68|
|Water table at 8–10 m||Drooping||24-I-68|
|Refresco||3–5 cm thin salt crust||Fastigiate||24-I-68|
|Water table at 12 m||Fastigiate||18-VII-68|
|Tirana||Natural forest, sand.||Fastigiate||26-III-69|
|Cortina||20-cm-thick salt crust||Fastigiate||26-III-69|
|Water table at 10 m||Drooping||26-III-69|
|Water table at 8–14 m||Drooping||26-III-69|
|Victoria||Very loamy soil, 15-cm-thick salt crust||Fastigiate||26-III-69|
|Water table at 2 m||Fastigiate||18-VII-69|
|Santa María||Natural stand||Fastigiate||18-VII-69|
|Sand without salt crust||Drooping||18-VII-69|
|Canchones||Sand, trees under constant irrigation id above, but without irrigation since 1973||Fastigiate||18-I-67|
|Caldera||Sand, near sea shore||3-year-old tree||01-IX-69|
|Santiago||Greenhouse with irrigation||Seedling||04-V-71|
|Santiago||Loam-silt soil with scant irrigation||Fastigiate||20-XI-83|
Epidermis. The epidermis is covered by a cuticle of varying thickness (2.5 to 10μ). Epidermal cells show irregularities both in shape and size, and can be triangular, rectangular or irregularly polyhedrical. It must be pointed out that they are easily dyed with the dyestuffs used. Occasionally, in greater or smaller numbers, a spherical body that does not become dyed is observed within the cytoplasm.
The adaxial face presents an average of 200 stomata per mm2 and the abaxial face 120 stomata/mm2. Hull & Bleckmann (1977) give figures of 217 and 97/mm2, respectively, for seedlings raised under greenhouse conditions.
The stomata are slightly sunk in the epidermis of both faces, and may or may not be complemented by subsidiary cells in actinocitic or paracitic arrangements (Esau, 1965) on the adaxial and abaxial face, respectively (Figure 2).
Figure 2. Stomata: A. adaxial, actinocitic arrangement; B. abaxial, paracitic arragement. The number and organization of the subsidiary cells differs between both stomata.
Under the epidermis, and closely related to it, as if it were their own extension, there are sub-epidermal cells characterized by their transparency and lack of affinity with the dyestuffs.
Mesophyll. As a result of its isolateral structure, the palisade tissue in tamarugo folioles is organized under both epidermis. It is formed by three to five layers of elongated cells which bear the chloroplast, being those on the adaxial face slightly longer and narrower (minimum and maximum lengths of 30 to 50 μ and width 6 to 8 μ), than those on the abaxial face (16–24 μ long and 8 to 12 μ wide).
It is very striking to find, among the palisade cells, conic-shaped cells of larger size (Fig. 1), hereinafter referred to as “special cells” (S.C.), which, like epidermal cells, become heavily dyed with the dyestuffs used. It is worth mentioning that when potassium iodine or Schultze solution are used, their walls do not acquire the characteristic yellow or blue color, respectively, typical of cellulose (Raulin & Takahashi, 1952). These cells are formed by a single element or by 2 to 4 segments, as may be seen in Figure 1.
The S.C., possibly, correspond to the most peculiar characteristics of the foliole anatomy. Their size is always larger than that of palisade cells and their number varies greatly, exceeding even occasionally that for palisade cells, particularly at the adaxial face and, preferably, under the central conductor bundle of the abaxial face. Their presence has been difficult to correlate with any of the analyzed parameters.
The mesophyll, save for certain exceptions, is compact and lacks intercellular spaces, and the cells among the palisade tissue, when present, are represented by some large thin-walled isodiametric cells, with scant or no chloroplast.
Conductor tissue. It is made up by collateral bundles, but often the phloem at the central bundle is more prominent than the xylem, surrounding it almost completely, thus being it a semi-amphicrib type of structure. It is possible that the resistance tissue is represented by colenchyma or fibers, the walls of which may be thin or very prominent. Both in the phloem and the xylem there are idioblasts with polygonal crystals and other idioblasts, less abundant, which contain certain substances that take up the dyestuff of the S.C. The vessels and tracheids are of the ring-like type.
Another fact worth mentioning is the presence of a bundle sheath formed by isodiametric cells which become as strongly dyed as the special cells and, as in their case, the cell wall thickness is not possible to measure. This feature, together with the fact that they continue on to the little bundles, makes it difficult to define them as typical Kranz cells (Hattersley & Browing 1981) or “distinctive cells” (Tateoka, 1958).
Anatomy of the developing foliole. Developing folioles, save for a few exceptions, do not show morphological differences visible at the structural level (Pictures 1 and 13), as they only become noticeable afterwards.
Their main features are to be totally isolateral, with a thin cuticle (0.10 to 0.15μ), lacking sub-epidermal and special cells. The cells which would constitute the bundle sheath are transparent, apparently devoid of chloroplast and lacking dyestuff relationship.
Tamarugo may not be classified as a strictly deciduous tree, as its leaves are continuously being shed and simultaneously renewed throughout the year. This means that, after the great springtime outburst, new leaves sprout to replace those in continucus abscition. Solely when winter temperatures are extremely low (-5 to -7° C), it sheds its leaves completely. Otherwise, as observed in 1969 (Table 1), the trees maintain their ability to develop new leaves. This situation makes research considerably more complex, as when the leaf samples were collected this feature was not taken into consideration, since the main purpose of this study, stemming from previous observations, was to find possible correlations between environment and morphology. However, when the collected samples were analyzed, it was realized that the age of the leaf and the collection date were also important data.
Leaf morphology has been studied particularly from the standpoint of its efficiency in capturing energy and of the resistance which its tissues may oppose to water loss. However, not all xeric adaptations protect plants against water loss, and not all modifications in xeromorphism are related to xeric habits (Sudzuki 1982).
A number of recent ecophysiological studies are oriented towards establishing the effects of the environment on leaf morphology and its relationship with the physiological behaviour (Smith & Nobel 1977, 1977b and 1978; Chabot & Chabot 1977; Berlin et al. 1982; Cutter, Rains & Loomis 1977).
Turner and Begg (1981) are of the opinion that plants should be selected basing on their ability to adapt to impredictable deficits. Berlin et al. (1982) consider that plants, unquestionably, respond to water differences in a number of ways depending on the environmental conditions, and that these not only provoke morphological modifications, but also influence the structure of certain cytoplasmatic organules (mitochondria, peroxisome, etc.). Likewise, Van Volkenburg and Davies (1977) consider that the foliar structure is modified by changes in the environmental conditions and that these modified structures characterize the water relations and other physiological processes. According to Harris & Cambell (1981), desert plants can live only if they have the capacity for quickly developing physiological and morphological adaptations enabling them to acclimatize themselves to the harsh conditions prevailing in the desert, an environment typically presenting the widest ranges of climatic unevenness.
The analysis of the collected material showed that:
no morphologic differences were observed between the folioles from fastigiate and drooping plants;
in general terms, foliole anatomy is closely related with its developmental stage, and
the material from the Tamarugal Pampa shows certain differences among its own samples, but these differences become much more marked when compared with the material collected at San Pedro de Atacama, Santiago and Caldera.
Summary of the most important characteristics observed in the anatomy of tamarugo leaf folioles. Sites are arranged according to depth of the groundwater table; general data on the type of soil and presence of surface salt crust is also provided. Only anatomic features selected are cuticle thickness and presence of sub-epidermic cells. Some characteristics of the special cells (S.C.) are included.
|Superficial water table 2–4 m||Type of soil||Salt crust thickness (cm)||Date month||Cuticle thickness μ||Sub-epidermal cells (*)||S.C. (**) Characteristics|
|Quillagua||sandy-loamy||No||XII-68||5–7||2/3–1/2||Not seg. 4:5|
|Barreda||sandy-loamy||No||XII-68||9–10||2/3||Not seg. 4:3|
|VII-69||4–5||Not visible||Seg. 4:2 Perforated|
|Recreo||loamy||No||III||3–4||1/2||Not seg. 3:4 Perforated|
|Sulfatera||loamy||No||XII-68||3.5–9||1/3–2/3||Not seg. 11:10|
(*) The fraction entered corresponds to the ratio between its depth and that of its corresponding epidermal cell.
(**) Not seg. = not segmented, i.e., formed by a single cell. The ratio corresponds to the average number of S.C. for the adaxial and abaxial epidermis, respectively, within 1 linear mm.
|Mid-depth water table||Type of soil||Salt crust thickness (cm)||Date month||Cuticle thickness μ||Sub-epidermal cells||S.C. Characteristics|
|Canchones (*)||sand||No||IX-67||4–5||Not visible||Not seg. 1:0|
|IX-83||4–5||Not visible||Not seg. 9:7|
|Junoy||Loamy-sandy||7–15||III-I y||2.5–5||Scant||Not seg. 10–9 Perforated|
|VII-69||2.5–5||1/2||Not seg. 5–4 Perforated|
|Refresco||Loamy-sandy||7–15||I-68||2.5–5||1/2–2/3||Not seg. 3:2|
|VII-68||5–7.5||Scant||Not seg. 5:13|
|Gatica||Loamy-sandy||40||I-68||6–7||Not visible||Not seg. 3:6|
|VII-69||4–5||Not visible||Not seg. 5:4 Perforated|
|Cortina||Loamy-sandy||40||I-69||2.5–4||Not visible||Not seg. 5:4|
|Deep water table|
|Sta. Emilia||sand||No||XII-69||2.5–3||1/4||Seg. 2:4|
|VII-69||2.5–6||2/3||Not seg. 5:2 Perforated|
|Sta. María||sand||No||VII-69||3–5||Scant||Not seg. 2:0|
(*) The large difference between both samples is derived particularly from the greater amount of S.C. in the samples collected in IX-83. Refer to the text.
The situation of the material collected at San Pedro de Atacama, Santiago and Caldera is analized in the text.
XII-I = Summertime, characterized by high nocturnal relative moisture (R.M.) %.
VII = Winter, normally with lower R.M. % and nocturnal temperatures.
Table 2, which groups the material collected at the Pampa according to groundwater table depth at the sites where the trees were growing, shows a summary of the general similarities and differences of the most relevant parameters. As can be seen, neither the water table depth, the quality of the soil nor the collection date have a notorious influence on the morphological characteristics considered. Nevertheless, there are some remarkable modifications, which may be tentatively attributable more to differences in the developmental stage of the foliole than to environmental factors. This situation may be due particularly to the feature described above, that on account of the peculiar foliar development of tamarugo, being neither deciduous nor evergreen, the entire range of developmental stages can be found at any one given time, and the lack of major differences may be due to the fact that all the Pampa locations included in Table 2 have the same climatic conditions.
The developmental stages of the tamarugo folioles analyzed can be summarized into three groups:
Juvenile stage: The juvenile stage foliole (Picture 1) is characterized by being totally isolateral, having a relatively thin cuticle (2–3 μ), prominent epidermic cells with poor dyestuff relationship, and by lacking sub-epidermal and special cells. Bundle sheath cells are isodiametric and, despite their lack of dyestuff relationship, no cytoplasmatic organules were observed with the optical microscope used.
Adult stage: As the folioles develop, and probably depending on the prevailing climate, the anatomic pecularities of this species start to become evident. The foliole can reach a length of 8–9 mm and a width of 2 mm, or stay as small as 4–5 mm long and 1 to 1.5 mm wide (thickness measurements were insufficient). Possibly, this variation in foliole size is related to the luminosity and humidity prevailing in the area (Smith & Nobel 1977) during their developing period.
Tamarugo folioles are glabrous, save for exceptional cases where a micrometric hair may be observed. The foliole surface, though normally smooth, may become corrugated up to the point where complex folds become predominant (Picture 2), including the cuticle which acquires prominent shapes. These epidermal and cuticle structures are possibly related to more efficient water use, helping to avoid heat buildup in the leaf.
The adult foliole cuticle may be either very thin or extremely thick (Picture 3, Table 2).
The cuticle was regarded as an organization especially structured to control transpiration (Hamilton 1975). However, Meidner (1954), with Cristaria aristata, and Bhatt and Lahiri (1964), with Prosopis spicigera, have found certain evidence of water absorption by the leaves. Hull (1966, 1970) and Hull & Wharrie (1975) studied the structure of the leaves and their capacity to absorb organic substances, pesticides and other compounds. Furthermore, Hull et al. (1979) are of the opinion that the unusual epicuticular configuration in Prosopis tamarugo, with vertically arranged ceraceous plaques that are not affected by ambient luminosity, could correspond to an adaptation mechanism by means of which the plant improves its water balance and, consequently, the capacity to thrive under xeric conditions.
The study of the collected samples revealed a variation in cuticle thickness, but no correlation was found for thickness and sampling date and place, possibly due to insufficient data or to the organization of the collection of the studied material.
Epidermal cells start to show some affinity with the dyestuffs as they grow older, and in some preparations the presence of a spherical corpuscle that does not become dyed may be observed (alcalloid corpuscle?); there is rarely more than one, and if there are more, they are small. At the same time, the presence of cells that do not become dyed may be observed in many preparations, which we have considered as structuring a sub-epidermis (Picture 3). These sub-epidermal cells, in some cases, only occur under the adaxial epidermis and, in other cases, when they are very prominent, under both faces.
The occurrence of sub-epidermal cells is seemingly closely related to the age of the foliole, as they cannot be found in developing or immature folioles. They become subsequently more notorious —while the epidermal cells become more reduced in size— up to such a point that the sub-epidermal cells get to be one-third to two-thirds more voluminous than the epidermal cells. These cells, which occur coincidentally with each epidermal cell, never occur under the subsidiary cells of the stomata.
Another peculiar feature of the sub-epidermal cells is their total lack of dyestuff relationship, which makes them easy to detect by the high contrast they offer with the strongly dyed epidermal cells (Picture 3). Despite their lack of affinity with the dyestuffs, no kind of cytoplasmatic organules or structures could be observed with the optical microscope used.
A series of changes could be detected at the mesophyll, such as the length of the palisade cells, number and structure of the S.C. and presence or absence of intercellular spaces.
According to Berlin et al. (1982), the palisade cells in cotton plants subjected to water stress had the same diameter, but were more elongated than those of irrigated plants in which intercellular spaces had not been altered. The presence of extremely elongated palisade cells was observed in some preparations from the Junoy Forest in samples collected in March 1969.
As regards the intercellular spaces, they were normally absent or very scant, except in the remarkable cases of plants developed under irrigation in Santiago (Picture 16), immature and mature folioles from San Pedro de Atacama (Pictures 10 and 11), certain adult leaves from Caldera (Picture 14) and Canchones plants under irrigation (Picture 8). These cases suggest a relationship between the presence of intercellular spaces and the water regime under which the tamarugo plants are growing.
It is also in adult folioles where the S.C. are clearly differentiated, the number, size and structure of which (single or segmented) (Pictures 4–5) are greatly variable (Table 2). There appears to be a correlation with the water regime, since their numbers decrease notoriously when the tree is subjected to irrigation, as in the case of plants raised in a greenhouse (Picture 16). The most remarkable example is provided by tamarugo trees growing next to an orchard receiving constant irrigation in Canchones, the folioles of which showed nearly none of these cells (Table 2 and Picture 8). But, subsequently, in 1983, these trees, whose irrigation had been suspended in 1973, showed as a major difference the presence of abundant numbers of these S.C. (Table 2 and Picture 9).
The great amount of mucilage contained in the tamarugo leaf is nestled in the epidermal cells and in the S.C., which supports the assumption, together with the above, that they are possibly helping in water absorption from the atmosphere, as with their matric potential they contribute to increase the high water potential detected in this species by Sudzuki, Botti & Acevedo (1973).
The conductor tissue also appears affected, but no correlation could be found with the parameters analyzed. In some cases the bundle sheath (“distinctive” or Kranz cells) surrounds completely the central vascular bundle (Picture 6); in others, preferably on the abaxial side. However, the secondary nervation, in general, is totally surrounded by this special type of cells.
The intense studies being conducted around the photosynthetic mechanism and the correspondence between the type of photosynthesis and foliar anatomy has given rise to the interest in the knowledge of the environmental influence on the individual foliar morphology.
According to Hattersley (1984), there are anatomic contrasts among the types of photosynthesis and the ratios of the area of the mesophyll of C4 plants (PCA), the “Kranz” tissue (PCR), or that of the bundle sheath (PBC of the C3 plants) per vein, and that this proportion is somehow related with the position in the leaf and probably with the environmental conditions prevailing during the growth of the leaf.
Senescent stage: The old folioles show a peculiar modification: both the special and the mesophyll cells present “perforations” (?) in their walls (Picture 7). These perforations or “digestibility” or “cytoplasmatic transformation” may also be observed at the epidermic cells. What is the function of these cells? An in-depth study of its morphology and contents might possibly help to understand their function in the extraordinary efficiency in water economy typical of this species.
TAMARUGOS GROWN OUTSIDE THE TAMARUGAL PAMPA
a. San Pedro de Atacama
The greatest differences were found for leaves of tamarugo growing under different conditions than those prevailing at the Pampa (Table 3). Pictures 10 and 11 show the structure of a developing foliole and that from an adult tree growing at San Pedro de Atacama. As may be seen, they are very different from the Canchones folioles (Picture 1), particularly as regards the development of the stomata and the disposition of the mesophyll in the young leaf. Picture 11, of a young leaf, shows that the intercellular spaces remain unaltered. It must be pointed out that in San Pedro de Atacama rainfall averages 19 mm and the temperatures are lower than at the other locations studied (Table 3).
Smith and Nobel (1978), working with Encefalia farinosa, established that, besides the influence of the water on foliar development, luminosity would also act in the internal/external area ratio (Amonth/A) and that the soil potential which affects the size of the leaf, the growth rate and the hydric condition, secondarily influences the Amonth/A ratio. According to the observations made in Canchones, Caldera and San Pedro de Atacama folioles, luminosity possibly has an influence in the size and internal morphology of tamarugo folioles.
Some meteorological data characterizing San Pedro de Atacama, Caldera and Canchones. Relative humidity is not included, to avoid confusion, as the relevant data are the maximum readings, periodicity and time of reading.
|Location||Luminosity||Cloudiness *||Temperatures ° C||Average rainfall|
|San Pedro de Atacama 2.436 m asl, 68° 20' W||519.8||Insufficient data||17.9||6.6||27.9||-2.5||19.1|
|Caldera 10 m asl 70° 50' W||368.8||100.7||43.5||20||12||25.2||9.5||36.4|
|Canchones 1,200 m asl||551.0||33.0||226.0||30.9||4.6||36.0||-6.6||0.6|
|Santiago 520 m asl||206.4||78.0||152.3||22.2||7.8||36.3||-4.6||366.8|
* On the basis of 1/8 of the skies. The remaining days in the year correspond to skies with less than 6/8 cloudiness; clear days are those with 0 cloudiness.
asl = above sea level
The most dramatic case is that shown by tamarugo plants at the Caldera plantations. Caldera is a land strip on the seashore, with long foggy periods (Table 3) and an average relative humidity of 82%. These plantations failed because the tamarugo trees died at the third year. Pictures 12, 13 and 14 show three different anatomies of leaves sampled at three-year-old tamarugo from plantations growing at Caldera.
A possible explanation for this fact could be as follows: According to the moderate temperatures occurring at the area, these plants ought not to shed their leaves, and during the long fog season (May to September) they developed leaves of the “hydric” type, remarkable for their considerable size and thickness. These leaves, which were not adapted to the strong sunlight (Smith & Nobel 1977b), were destroyed —as could be observed— during the luminous period. Drawing on the reserves, the plants raised new leaves to replace the dead ones, this time adapted to the luminous conditions, but which, when the environmental conditions changed again, were once more destroyed. Under these circumstances, if we assume that the plants absorb environmental moisture and translocate it to the root mass and then exude it to the ground —which in this area is a thick sand layer with no water holding capacity—, the plants would be forced to deplete their reserves to form new foliage without counting on enough moisture stored at the rhizosphere. It is logical to think that under such circumstances the seedlings would have to die out of depletion of their reserves and whithering from not having leaves to carry out the photosynthesis, at the same time as supplying water to the root system at the moment when it was most needed.
Pictures 15 and 16 show a developing and an adult foliole, respectively, of tamarugo trees grown in a greenhouse in Santiago with 16° C night temperature and 25° C daytime temperature (± 2° C) and irrigation when needed. Doubtlessly, these temperatures and the greenhouse luminosity could not alter the foliole morphology at its first developmental stages (compare with Picture 1), but they did alter the adult foliole. At this stage the foliole has a totally different anatomy from that typical of tamarugo (Picture 6), since it has no S.C., it is bifaced and has abundant intercellular spaces. The bundle sheath can be made out, but only its walls become dyed, not its cytoplasmatic content.
It may be stated that a systematic and in-depth research study is mandatory on the anatomy and physiology of this fascinating species, which can thrive under such harsh environmental conditions for any plant species as those found at the Tamarugal Pampa.
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Foliole in juvenile stage from a plant grown at Canchones (I-1967). 100 ×.
Adult foliole with very undulated surface, regular number of S.C. and bundle sheath cells not very prominent in the central nerve but notorious in the secondary nerves. Place of collection: Victoria. (III-1969) 100 x.
Thick cuticle (10 μ), overdyed epidermal cells and subepidermal cells which do not become dyed. Sample from the Yamará forest (XII-1969) × 400.
Palisade cells (thin) and S.C. (thick). Observations made with scan microscope. IX-1983. × 305. Kindness of the Faculty of Sciences of the University of Chile.
Detail of a segmented S.C. seen in a scan microscope. IX-1983. × 1220. Kindness of the Faculty of Sciences of the University of Chile.
Conductor bundle surrounded by bundle sheath cells, presence of crystals and idioblasts with substances which take up the dyestuff of the S.C. In this case the phloem is protected by colenchyma. The presence of numerous flat S.C. may be observed. La Tirana, III-1969. × 400, contrasted phase microscope.
Leaf in senescent stage. It is characterized by the destruction of walls (or cytoplasm?) in the epidermal cells, S.C. and bundle sheath. VII-1969 × 100.
Tamarugo foliole from a tree growing at Canchones under constant irrigation. The presence of abundant intercellular spaces and absence of S.C. may be observed (IX-1969) × 200.
Foliole from tamarugo growing in Canchones at the same place as that in Picture 7, but which irrigation was discontinued for ten years. The cuticle, the presence of epidermal cells and abundant S.C. are notorious. IX-1983. × 100.
Young foliole from a tamarugo leaf growing at San Pedro de Atacama. Note the peculiar structure of the stomata and mesophyll. III-1969. × 200.
Foliole from leaves collected at San Pedro de Atacama. They present a thick cuticle, scant S.C., abundant intercellular spaces and characteristic bundle sheath cells, the intervenal ones particularly well developed. San Pedro de Atacama. III-1969. × 100.
Young foliole of tamarugo plants growing in Caldera, developed during a moist period. IX-1969. × 100.
Adult foliole from tamarugo growing at Caldera. IX-1969. × 100.
Another foliole from an adult leaf of tamarugo growing at Caldera. The amount of S.C. and intercellular spaces of the mesophyll is remarkable. Caldera. I-1969. × 100.
Young foliole from a plant grown under greenhouse conditions. No remarkable differences are observed. Santiago, V-1971. × 100.
Adult foliole from a tamarugo grown under greenhouse conditions without water deficit. The bilateral structure may be appreciated, with many intercellular spaces and absence of S.C. The bundle sheath cells can be made out easily, but they do not become dyed. Santiago. V-1971. × 100.