The Negev: The Challenge of a Desert, Second Edition [2nd ed. Reprint 2014] 9780674419254, 9780674419247

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The Negev The Challenge of a Desert

The Negev The Challenge of a Desert Second Edition Michael Evenari Leslie Shanan and Naphtali Tadmor with chapters by Yehoshua Itzhaki and Amiram Shkolnik

*

Harvard ü.n|v 4

k

>-

Τ

\ 30.71962

6.5.1962

k v «

19.2.1963

0

1

2

3 A

5cm

Fig. 155. Schematic drawings of one bean-caper plant (ZygophyJlum dumosum) in its natural habitat, representing its state of development at the various dates indicated: ^ l e a v e s with two blades; ( leaves with one blade; | petioles.

Table 32. Number of leaves and petioles and additional growth of the bean caper plant (Zygophyllum dumosum) shown in Fig. 155; combined length of all branches at start of observations, 147 mm. No. of leaves with blades

No. of petioles without blades

Additional growth of all branches (mm)

Year

Rainfall 3 (mm)

1962

64

May June

22 0

20 31

11

1963

29

February April July November

0 19 0 0

25 25 35 25

o

February June

31 0

18 34

29

1964

a

183

Month

F o r previous rainy season; for example, 64 mm in 1961-62.

Adaptation

of Plants to Desert Conditions. I | 253

explains w h y they remain d w a r f y even after 200-300 years. The bean-caper plant after 250 years of growth, for example, is still no taller than 50-70 centimeters and has a crown diameter of only 90-100 centimeters. After the unusually a b u n d a n t rainfall of 1963-64 a bean-caper plant that w e studied added to the 147-millimeter combined length of its main stem and existing branches only 29 millimeters of n e w p e r m a n e n t growth. Its most vigorous branch grew a mere 5 millimeters—and this in a good rainfall year! Is this slow growth a constitutional feature of the dwarf shrubs or is it a consequence of summer drought? We f o u n d the answer by irrigating in a dry season some of the dwarf shrubs growing at Avdat and comparing them with unirrigated dwarf shrubs growing under exactly the same climatic conditions. In one case the m a i n stem of an irrigated bean caper grew in 10 months f r o m 19 to 482 millimeters, excluding the growth of the m a n y newly f o r m e d side branches (Fig. 156). This clearly indicates that if sufficient water is m a d e available to them the real growth potential of the xerophytic dwarf shrubs is a f e w h u n d r e d times greater t h a n their normal growth under natural desert conditions. Under natural conditions the plant regulates its growth in accordance with the amount of available water. If this amount is insufficient, the plant slows d o w n its growth and under extreme critical moisture stresses will die. This death by starvation has an additional interesting aspect. It often h a p p e n s that not the whole plant but only some of its branches die. Other branches retain just as m u c h green photosynthesizing matter as can be supplied with the available water and this suffices to keep a f e w branches alive (Fig. 157). Sometimes in extremely dry localities in years of great drought only a single branch out of m a n y survives in this way. During the following years the plants may slowly regenerate themselves f r o m dormant renewal buds. This is a fascinating phen o m e n o n w h i c h shows that, paradoxically, w h e n death is partial it becomes a m e a n s of survival. Survival through partial death is possible only because the individual branches of the plants concerned possess a great degree of physiological independence—a fact proved also by another typical feature of some desert dwarf shrubs. The originally undivided stem of a mother plant developing f r o m the main axis of the seedling can split into several daughter stems w h i c h are either loosely attached to one another or completely separated (Fig. 158). In the stem of the bean caper, for instance, splitting is accomplished because during secondary radial growth of the stems the cambium, instead of forming annual rings, ceases to be active in certain areas. It continues to divide only in arcuate stem segments w h i c h grow radially and form longitudinal strips along the stems. The stems therefore grow in thickness only in certain parts of their circumference and become ridged. Since in those sections in w h i c h the c a m b i u m becomes inactive the original tissues die, the stems split into a n u m b e r of autonomous entities, each with its o w n root system and water supply, loosely held together only at their base.

254 I The Negev

Fig. 156. Schematic drawings of an irrigated bean-caper plant (ZygophyJIum dumosum) growing next to the unirrigated plant depicted in Fig. 155. Of the many side branches only F, G, H, and I are fully drawn. 1 flowers; other symbols as in Fig. 155.

V N . ,> 0 1 2 3 A 5cm

ψ

Fig. 157. A bean-caper plant (Zygophyllum (arrow) in the process of splitting.

dumosum)

with one branch

Fig. 158. A bean-caper plant (Zygophyllum dumosum) in a drought year. Only a few branches (on the right) carry very few leaves; most of the branches are dead.

256 I The Negev Another m e a n s that the summer-active xerophytes use to balance their water economy is to reduce the amount of water lost by their transpiring surface. This reduction of the transpiration rate (water lost per unit surface or unit weight) can be very great. In the case of the articulate saltwood or the tubercled rue ( H a p l o phyllum tuberculatum), for example (Table 33), transpiration rates during the dry season amount to only 27 and 20 percent, respectively, of the spring values. We have f o u n d that other plants are less efficient. In some cases the seasonal reduction of the transpiration rate is due to the fact that the transpiring organs of the plant during the rainy and the dry seasons are not identical. The bean caper will again serve as an example. We have mentioned that the bean

Fig. 159. T r a n s p i r a t i o n rates: (a) of leaf blades, (b) of b l a d e l e s s peti o l e s that still h a v e their original structure (see Fig. 154a), a n d (c) of a n a t o m i c a l l y c h a n g e d b l a d e l e s s p e t i o l e s (see Fig. 154b) of a b e a n - c a p e r plant ( Z y g o p h y l l u m d u m o s u m ) . T h e t r a n s p i r a t i o n rates ( m i l l i g r a m s of w a t e r lost b y transpiration b y 1 g of f r e s h w e i g h t of plant in 1 min) w e r e m e a s u r e d s i m u l t a n e o u s l y o n a s u n n y N o v e m b e r day. A r r o w i n d i c a t e s t i m e of s u n s e t .

Hrs.

Table 33. S e a s o n a l r e d u c t i o n of transpiration: ratio (percent) of t r a n s p i r a t i o n rate during dry s e a s o n to that during spring.

Plant Gray-leaved sagebrush (Artemisia herba aJba) Round-leaved heliotrope (Heiiotropium rotundifolium) White broom (Retama roetam) Bean caper (Zygophyilum dumosum) Saltbush (Atriplex haJimus) Jointed saltwood (Haloxylon articulatum) Tubercled rue (Hapiophyilum tuberculatum)

Transpiration ratio (percent) 73 65 48 47 31 27 20

Adaptation

of Plants to Desert Conditions.

I | 257

caper loses its leaf blades during summer and that the remaining petiole undergoes considerable anatomical changes (Fig. 154). When the transpiration of blades, unchanged petioles, and anatomically changed petioles is tested under the same environmental conditions, the reduced transpiration rate due to the loss of the blades and the altered structure of the petioles is easily verified (Fig. 159). The same reduction is found when the transpiration rates of winter and summer leaves of the gray sagebrush are compared. So far we have considered only the reduction during summer of the transpiring surface and transpiration rate of the shrubs and dwarf shrubs that are active during the dry season. The real importance of these factors for the survival of these plants can be best appreciated if the water loss for a whole plant is calculated for each month of the year. Only then does the enormous efficacy of the combined action of reduction of transpiring surface, seasonal decrease of transpiration rate, and morphologicalanatomical change of the transpiring organs become obvious (Table 34). The white broom, the round-leaved heliotrope, and the tubercled rue cut down their water output during the dry season to 1.8, 3.5, and 2.2 percent of their maximal values, figures that clearly indicate the outstanding adaptability of these summer-active xerophytes to the water conditions of their habitats. This is even more remarkable since these three plants are morphologically, anatomically, and taxonomically very different. The broom (pea family) is leafless, the heliotrope (borage family) has relatively large leaves, and the rue (rue family) possesses small leaves. Nevertheless, under the harsh dry conditions of the desert summer there are occasions when all these ingenious devices of the summer-active xerophytes for regulating their water economy are still insufficient to balance intake and output, even when there is still plenty of available water in the soil. On a chamssin day with temperatures between 40 and 45 °C, water loss by transpiration is high. Even if there is ample available soil moisture, the supply from the soil often fails to keep pace with the water output, resulting in a temporary deficit. The situation, however, is rectified during the night hours. At night transpiration is negligible, but water intake from the soil continues and the plant will recover its loss by reaching full saturation, ready to start the next day with an internally balanced water budget. These deficits are therefore transient, but with increasing drought and decreasing available soil moisture the plant is less and less able to recover its losses, which accumulate from day to day. In the world of finance, when a certain lower limit has been exceeded, accumulating deficits lead to bankruptcy, but in this particular plant world most of the summer-active xerophytes can tolerate very considerable water losses during the dry season without reaching the level of bankruptcy (Table 35)—a factor to which they partly owe their survival in an active state.

258 I The

Negev

Table 34. Monthly output of water for whole plants.

Aaronsohnia

faktorovskiia

Month

Rainfall (mm)

Ave. output (kg/ plant)

Percent of m a x . output

Desert mignonette (Reseda muricata)b

Toadflax (Linaria h aeíava)a Ave. output (kg/ plant)

Jan.

7.0

0.2

50

0.03

Feb.

74.5

0.4

100

0.2

Mar.

4.0

0.2

50

0.12

Apr.

9.0

—

—

—

May

0

—

—

—

June

0

—

—

July Aug.

0

—

0

Percent of m a x . output

Ave. output (kg/ plant)

Percent of m a x . output

15

0.4

100

4.6

76

60

6.1

100

—

3.0

50

—

0.9

15

—

—

—

—

—

—

—

—

—

—

—

—

—

—

65

—

Sept.

0

—

—

—

—

—

—

Oct.

0

—

—

—

—

—

—

Nov.

4.5

—

—

—

—

0.2

3.3

Dec.

8.5

—

—

—

—

0.065

1.1

W i n t e r annual. S u m m e r - i n a c t i v e perennial. 0 S u m m e r - a c t i v e perennial. a

b

The balance sheet of any economic system has a debit and a credit side. Up to now we have considered only the debit side of the water economy of xerophytes. How does the credit side look, that is, what are the plant's water sources and how do they exploit them? Since dew as a water supply is of no importance for higher desert plants, they must rely on available soil moisture which is taken up through the roots. The roots of desert shrubs and dwarf shrubs are specially adapted to the moisture conditions of their habitats. When growing on hilltops, slopes, or loessial plains their root systems are very shallow and do not penetrate to more than 30-50 centimeters (Fig. 160), since either deeper soil is lacking or the deeper layers are permanently dry. The lateral extension of the root system, however, is enormous, and out of all proportion to the size of the plants. In a typical stand of relatively young plants of the bean caper the lateral roots extend over an area of 4-7 square meters, whereas the plant parts above ground cover not more than 0.4-0.5 square meter. The figures for much older plants may go up to 30-35 square meters for the roots and 1.5-2 square meters for the parts above ground (Fig. 160). Consequently the ratio of weight of the whole root system to weight of the shoots above ground is very high. This means that each unit of transpiring surface is supplied with water by many more roots than is usual in nonxeric environments. Shrubs growing in loessial or gravelly wadis where water is found at deeper layers have roots penetrating to depths of 2-4 meters and more (Fig. 161c). Some of these shrubs, for example, the white broom (Fig. 160, lower), have it both ways: the main

Adaptation of Plants to Desert Conditions. I | 259

Gray-leaved storksbill (Erodium giaucophyllum)b Ave. output (kg/ plant)

Percent of max. output

0.9 4.5 7.2 4.1 1.6

12.5 62 100 51 22

0.6 0.75

8.3 10.5

White broom (Retama raetam)"

Round-leaved heliotrope (Heiiotropium rotundifolium) c

Tubercled rue (HapJophyilum tuberculatum)c

Ave. output (kg/ plant)

Percent of max. output

Ave. output (kg/ plant)

Percent of max. output

Ave. output (kg/ plant)

Percent of max. output

180 350 380 360 108 23 9 10 11 7 21 130

47 92 100 95 28 6.1 2.4 2.6 2.9 1.8 5.5 34

1.2 5.6 6.1 7.5 1.8 0.55 0.6 0.4 0.34 0.23 0.7 0.9

16 75 81 100 24 7.5 8 5.3 4.5 3.5 9.3 12

6.2 10.5 21.6 16.3 2.2 1.2 0.8 0.6 0.6 0.45 1.8 5.1

28.6 48.5 100 80 10.2 5.5 4.2 2.8 2.8 2.2 8.3 26.5

Table 35. Maximal nonlethal water-saturation deficit (percent of maximal water content). Plant White broom (Retama raetam) Desert mignonette (Reseda muri cata) Gray leaved storksbill (Erodium giaucophyllum) Round leaved heliotrope (Heiiotropium rotundifoiium) Tubercled rue (Haplophyllum tuberculatum) Bean caper (ZygophyJIum dumosum) Saltbush (Atriplex haJimus)

Deficit (percent) 47 52 59 54 75 45 78

roots penetrate into depth, whereas the upper lateral roots are superficial and extend over a large area. In the relatively large living space taken up by the roots of each individual there is little or no competition for water among the perennials occupying the same habitat, although such competition is very common under less arid conditions, where shrubs grow at much closer spacings. The roots of all xerophytes tested have two attributes that to some extent conflict with the generally accepted knowledge of roots. Even the old parts of the roots, which are lignified and covered by cork layers, form young rootlets with greatest rapidity whenever the surrounding soil is wet. It is therefore the total root system that takes up water, not only its young parts. The roothairs, which are the most active water-absorbing elements, cover the young roots from base to tip and, contrary to what most botanical textbooks say, are not restricted to a narrow zone above the growing points. They appear a few hours after the first rain. Moreover, the root systems of all the desert shrubs and dwarf

260 I The Negev

Fig. 161. Schematic drawing of root systems: (a) jointed saltwood (Haloxylon articulation) growing on a loessial plain; (b) jointed saltwood growing on the edge of a wadi; (c) shaggy sparrow wort (ThymeJaea hirsuta) growing in a loessial wadi bed; dimensions in centimeters. (After Tadmor, Orshan, and Rawitz.) Fig. 160. Schematic drawings of the root systems of (upper) the bean caper and (lower) the white broom; α-α' indicates the maximal extension of the above-ground parts; dimensions are in centimeters.

shrubs are notable for their extraordinary plasticity and adaptability. For example, the jointed saltwood (Haloxylon articulation) generally grows on loessial plains, w h e r e it has a shallow root system. But sometimes it is f o u n d on the edges of w a d i s and then its roots penetrate to considerable depth (Fig. 161a, b). One of the main targets of our endeavor to find out h o w plants meet the challenge of the desert w a s to determine their water sources. Therefore at regular intervals w e measured the water content of the soil beneath plants by using the normal procedure of taking out bulk samples near the plant's roots and analyzing them for water. The soil moisture content in A u g u s t - S e p t e m b e r was usually about 4-6 percent by weight. In this type of soil, soil moisture below 6-8 percent is unavailable to the plants because the roots are unable to extract the moisture surrounding the soil particles. Since dew w a s ruled out as a source, h o w could the summer-active plants manage to find enough water after the soil moisture h a d d r o p p e d below 4-6 percent? Only a microanalysis solved the riddle. The soil layer on hilltops and slopes contains a great quantity of stones (hamadas and h a m a d o i d slopes). W h e n we tested samples of very small amounts of soil beneath these stones we f o u n d that even in the driest season they still contained between 9 and 12 percent of water by weight (Fig. 162). These pockets are sought out by the fine rootlets and are the main providers of moisture during summer. It is clear therefore that the stoniness of desert soils, and especially of the desert pavement, is of the greatest biological importance not only in increasing the

Adaptation

of Plants to Desert Conditions.

I | 261

amount of water infiltrating into the soil (see Chapter IX) but in creating and preserving such water pockets. The cracks and fissures of the underlying bed rock also fill up with water and the roots penetrate into these cracks during the summer and exploit these sources. Now, survival of desert plants is dependent not only on their water economy and photosynthetic capability but also on their ability to establish themselves at the right time and in the right place. This is achieved through the manifold germination mechanisms of their seeds, which have also adapted themselves to the particular desert conditions. Perhaps the most exciting aspect of our biological desert research has been the discovery, step by step, of the full harmony between environment and germination behavior. For a number of years we recorded in detail the life cycles of most of the plants belonging to the three main dwarf-shrub associations. This included counting and measuring seed germination, seedling growth, mortality, and survival for a number of years in 1-meter-square observation plots. Some plots received varying amounts of artificial irrigation, especially in the summer season (Fig. 163), imitating supplemental and unseasonal rain. However, this artificial rain did not induce the germination of even one single seed of shrubs, dwarf shrubs, or any other desert plant, even w h e n the irrigation was quite considerable. Figure 163 shows, for example, this failure to induce germination for the sagebrush. It appears that these plants cannot be fooled into germinating by unnatural "summer rains." This is an obvious

Fig. 162. (a) Soil profile of a hilltop with a summer-active dwarf shrub and its roots exploiting water pockets below stones; (b) lower surface of single stone, showing a net of fine rootlets; (c) vertical section of stone with its water pocket. The figures indicate the water content (percent of dry weight) of the various soil layers in September.

20cm b

20cm C

262

I The Negev

Fig. 163. N u m b e r of germinating seeds and seedling survival of the gray-leaved sagebrush (Artemisia herba alba) and the u n a r m e d saltwort (Salsola inermis) on two 1 - m 2 plots. B l a c k columns, m o n t h l y average rainfall (mm) of e a c h rainy season (numbers a b o v e columns for 1961-1963, to right of column for 1963-64 and 1964-65, for w h i c h the n u m b e r on top is the rainfall of the month with most rain). A r r o w s and n u m b e r s a b o v e them indicate time and amount (mm) of artificial irrigation. In certain years seeds germinated at two or three different times. T h e graph gives the n u m b e r of surviving seedlings at each germination date for the u n a r m e d saltwort. T h e two n u m b e r s w i t h an e x c l a m a t i o n mark are the n u m b e r s of surviving seedlings of the grayleaved sagebrush at the end of 1965. mm 60 AO

69.5

29.5

64.7

129.6 •1834

20

50

25

300

42

86.5 J162.8

L

AL 1

SALSOLA

200 100

X · .-t-rt-f-M«3

140 120 100

A R T E M I SIA

100!

80 60 ¿0

20

ι

69.5

m 1961

Ii

J) m 1962

64.7

»-•»--Φ-···

21 Ii 1963 SQUARE 22/D

Ii

29.5

21 1962

II

ψ,/

M 1964

86.5

129.6 1834

3Π |I 1963 SQUARE 22/B

II

21 1965

•162.8

3Π 1964

Adaptation

of Plants to Desert Conditions.

I ] 263

adaptation to what Bünning has aptly called the "time structure of the environment." In the worst drought year, 1963, not one seed of the sagebrush germinated. Furthermore, during the two previous years when rainfall was below average, in one square no germination occurred whatsoever; in the other one only a few seeds germinated, but the seedlings died very soon (Fig. 163). On the other hand, germination during the two rainy years (1964 and 1965) was good and most if not all of the seedlings survived. However, we have never recorded a year of mass germination of seeds of the sagebrush so characteristic of the annual desert plants. Nevertheless, because of the very high survival rate of the relatively few seedlings, the sagebrush established itself permanently in the observation plots after the two rainy years. All the other desert dwarf shrubs behaved in a similar manner. These observations indicate that the seeds germinate and produce surviving seedlings only in certain specific years. Therefore the population of grown-up dwarf shrubs should be composed of individuals belonging to definite specific age groups, with agegroup gaps in between. This feature was fully confirmed when we determined the age of all the bean-caper plants growing on two 500-square-meter plots in a typical habitat. We determined the age of the plants by counting the annual increment rings of their stems, since only one ring is produced per year. The results are given in Fig. 164. The time intervals between the age groups indicate those drought years when either germination was poor or the few seedlings that managed to germinate subsequently died. These observations also indicate that the chances of successful germination and survival occur on an average once in 5-7 years and that this seems to be quite sufficient to enable the permanent dwarf-shrub population to remain dominant in its typical habitat. Fig. 164. Age g r o u p s of p l a n t s of t h e b e a n c a p e r (Zygophyllum d u m o s u m ) o n t w o plots; ordinate, age (yr) of plants; abscissas, n u m b e r of p l a n t s in t h e v a r i o u s age groups.

5

10

15

20

25

30

35

AO A5

50

55

264

I The

Negev

Fig. 165. An acacia tree (Acacia raddiana) background are the mountains of Jordan.

in the Arava valley. In the

Adaptation

of Plants to Desert Conditions.

I | 265

We now turn to the summer-active desert trees. Trees grow in deserts only in those habitats that possess a relatively ample all-year water supply so that the tree can build up and maintain a minimum "critical mass." Such habitats are the oases, the salt marshes, and some of the main wadis of the Negev. In the oases the groundwater table is reached by the tree roots. The road from Sedom to Elat through the Arava passes a number of such oases, which stand out in the bare landscape as green spots dominated by a number of trees whose homeland is originally tropical Africa. The most important are the toothbrush tree (Salvadora persica), the Egyptian balsam tree (Balanites aegyptiaca), the horseradish tree (Moringa aptera), and the doum palm ( H y p h a e n a thebaica), which is most conspicuous because in contrast to most palms it has a branched stem. These trees exist in these tropical enclaves far north of their center of distribution because of the very special physiographic conditions of the Arava rift valley, where temperatures are high (never below 0°C) and available groundwater accumulates in certain spots. They are best characterized by the Arab description of the date palm: "Their heads are in fire, but their feet in cool water." The permanently wet salt marshes and salines at the south end of the Dead Sea feature a luxuriant green vegetation, especially the tamarisks, which form junglelike thickets with their slender branches covered by small light-green leaves. At blossom time the violet-lilac flower spikes transform the salt marshes into veritable gardens. Here the ground is sometimes wet even during the dry season. The tamarisks spend water freely because their roots reach the highly saline water table (20 percent of salts and more), which, though poisonous to most plants, is harmless to the tamarisks perhaps because they possess special glands through which they excrete the surplus salts. We know eight different species of tamarisks growing in the salines of the Dead Sea and of the Arava, some of them endemic to the area. Some of the main wadis are another habitat in which trees can develop. The many wadis flowing from the east and west into the Arava valley are dotted with a large number of green acacia trees, contrasting sharply with the brown-yellow landscape. They belong to three different species: Acacia spirocarpa, A. negevensis, and A. raddiana (Fig. 165). The homeland of the acacia tree is the savannahs of Africa and they penetrated the Negev from the far south. Their transpiration rates are extremely high, reaching momentary peak values of 2500-3000 milligrams of water per hour per gram weight of leaf (mg/g hr). This figure means that their leaves lose in 1 hour more than three times the amount of water they contain. Such high transpiration rates are not unique in desert plants. The round-leaved heliotrope (Heiiotropium rotundifolium) and the tubercled rue (Haplophyllum tuberculatum) have peak rates of 2700 mg/g hr. But of all the Negev plants measured, only the acacias attain these high rates in the middle of the dry summer, whereas with the other plants this happens during the rainy winter season. The acacia trees also differ from shrubs and dwarf shrubs in two other respects: their daily transpiration rate

266 I The

Negev

does not show a midday depression during the dry season and their average monthly transpiration rate increases rather than decreases during summer. The acacias can do all this because they exploit any soil moisture in the gravelly wadis down to many meters deep, including the groundwater table. These trees are therefore good indicators of year-round water supply existing below ground surface. The acacias are distinguished by still another unusual feature. They are "evergreen" but not in the normal sense of this term. In summer, after new leaves have been formed, they shed their old leaves and even some of their branches. This phenomenon is part of their heritage from Africa, where there are summer rains. In the savannahs there they lose their old leaves during the dry summer and sprout new ones at the time of the autumn rains, and they have kept this habit under the very different conditions of the Negev. The depressions and gravelly wadis of the Negev highlands with residual water harbor another tree, the Atlantic pistachio (Pistacia atlantica; Fig. 166), which sheds its leaves at the beginning of the rainy and cold season. Unlike the tropical acacias it originated in the high plateau of Central Asia (Irano-Turanian region), and it infiltrated into the Negev from the north. The southern and northern boundary lines of the pistachio and the acacia just touch each other in the Negev. The leafless saxaul (Haloxylon persicum of the goosefoot family; Fig. 138) is another Irano-Turanian tree, a native of the steppes and deserts of south Russia and central Asia. In the Negev it has found a very special ecological niche on the interior sand dunes and sand fields where its roots reach the groundwater table. The last group of summer-active desert plants are the biseasonal annuals. In contrast to the hundreds of gaily colored annual plants that cover the desert ground during a good rainy season and die during April-May (winter annuals), the biseasonal annuals remain alive and active during summer. Only five species belong to this group, all of them of the goosefoot family, which in so many respects has its own most peculiar characteristic features. In the Negev the unarmed saltwort (Salsola inermis) and Volken's saltwort (S. volkensii) are the most important biseasonal annuals, since they penetrate farther south than the other three species. The unarmed saltwort inhabits hammadoid slopes, whence it invades any spot where man has destroyed the natural vegetation and disturbed the soil. Wherever a new road has been built, or a pipeline or cable laid, this plant immediately appears in enormous numbers. It occupies the newly created (ruderal) habitat, but after 2-3 years it disappears and the area is taken over by other plants. Volken's saltwort is more or less restricted to ruderal localities. The development cyle (see Fig. 173) of both these species starts with the germination of the dispersal unit 2 immediately after the 2 A dispersal unit is that entity which w h e n m a t u r e falls off the mother plant to propagate the species. It m a y be a seed, a fruit containing one or more seeds, or a part of the plant carrying m a n y fruits.

Adaptation

of Plants to Desert

Conditions.

I | 267

Fig. 166. A tree of the Atlantic pistachio (Pistacia atlantica) in a wadi of the Negev highlands. The terraces date back to the times of the Israelite Kingdom.

268

I The

Negev

Fig. 167. Seedlings of the unarmed saltwort (Salsola inermis) in the rosette stage.

Adaptation

of Plants to Desert Conditions. I | 269

first rain. The seedlings produce a rosette of highly succulent leaves and remain at this stage for most of the rainy season (Fig. 167). At the beginning of the dry season, when the winter annuals are dying, the stems of the saltworts start to elongate. The relatively large winter leaves are shed and new smaller summer leaves appear, which with increasing drought become more and more scalelike. The stems continue to grow until September. From July to October the plants flower and fruit. The ripe dispersal units are shed during October-November, ready to germinate with the first rain. They collect under their mother plant, from where they are partly dispersed by runoff water and floods. In the meantime the mother plant has died. Every year when we saw the unarmed saltwort developing and growing on the dry slopes during the hottest and dryest season we marveled anew at its astounding ability to be most active during summer. This is even more astonishing because, in contrast to the rooting behavior of the summer-active shrubs and trees, the root system of both saltwort species is quite small. We first thought that the biseasonal saltworts, like the lichens, use dew as a water source during summer. After a dewy night the whole plant is wet and the moisture is taken up by the leaves. The amounts of water thus provided are quite considerable, ranging from a minimum of 200 milligrams of dew per gram of fresh weight of the plant to a maximum of about 750 milligrams per gram. Even when no dew was formed during the night the relatively high humidity of the atmosphere furnished some small amount of water. But we found that dew absorbed during the night is insufficient to cover the loss of water by transpiration during the day. Even the largest amount that we ever measured was barely enough for 2 hours of early-morning transpiration (Fig. 168). Other summer-active plants also take up dew, but in no case did we find it an important water source. Another water source could have been dew ("subterranean dew") or water condensation in the soil. According to Boyko, this occurs in continental deserts and especially in sandy soils. We did not experience this process under our conditions. If it takes place—and this is possible—then the quantities of "subterranean dew" are so small that our equipment did not measure it. The source of water for these plants during summer is the same water pockets below stones that the roots of the dwarf shrubs survive on. In many other respects the basic drought-survival mechanisms of shrubs and biseasonal annuals are similar: they have a constitutionally small transpiring surface, and they also have the ability to reduce this surface area considerably during summer. Their transpiration rate also decreases during the dry season (Fig. 169). As long as the soil contains available water, their stornata are open the whole day, permitting full photosynthesis, with the relatively high peak of water loss being reached at noon. When soil water becomes scarce, the stornata are fully open only in the early-morning hours and transpiration sometimes falls to zero at noon.

270 I The Negev

Fig. 168. (a, b) Weight (mg) of two plants of the unarmed saltwort inermis) after a heavy dew night; from 18.30 hr of the previous night to 5.50 hr the following morning, 96 and 108 mg of dew had been formed on the two plants, (c) Transpiration rate (mg/gm hr) of one of these plants from 05.00 hr to 19.00 hr.

(Salsola

mg

Fig. 169. Transpiration rate (mg/g hr) of the unarmed saltwort (Salsola inermis): — winter leaves at the end of the wet season. (April 12); summer leaves after the winter leaves have been shed (July 28), from 05.00 hr to 17.00 hr.

Adaptation

of Plants to Desert Conditions.

I | 271

However much they may resemble one another in these features, dwarf shrubs and biseasonal annuals differ sharply in germination and seedling mortality. In some years the dispersal unit of both saltworts germinates in mass when conditions are favorable (Figs. 163 and 167). Even during the worst drought years there is still some germination. However, we were quite surprised to record that when a large number of dispersal units germinated the seedling mortality was high and few plants reached maturity and developed new dispersal units. In 1965, for example, with 162.8 millimeters of rain during the rainy season of 1964-65, over 300 dispersal units germinated in one square (Fig. 163). All of these soon died, in contrast to the situation in the preceding year when all nine of the seedlings that had germinated survived. The death of all these seedlings in the 1964-65 season is due to the competition for soil moisture between densely spaced seedlings, especially at the period when the soil starts to become dry. When relatively few seedlings are present there is less or no competition between them. As in the case of the sagebrush, artificial summer rains did not induce a single dispersal unit to germinate. There are some additional important points concerning germination of the biseasonal annuals that still need to be discussed. The survival of all annual species depends more than that of the perennials on the germination characteristics of their dispersal units, because each individual life cycle starts each year anew with germination. Under desert conditions, germination is therefore the most critical period of an annual's life cycle. Knowledge of the physiology and ecology of germination is indispensable for an understanding of the manner in which these plants manage to survive. The dispersal units of the unarmed saltwort contain in their outer parts a substance that inhibits germination. It is water soluble and has to be leached out before the dispersal units can germinate. This they do equally well in light or darkness over a temperature range of 5° to 30°C. When freed of their inhibitor, the freshly harvested dispersal units give 100-percent germination, but their life span is restricted. If stored they lose their viability; by the end of April only a very few will germinate and after a year their viability is nearly completely lost. The ecological implications are obvious. The mother plant sheds all the ripe dispersal units by November. The first heavy rainfall will leach out the inhibitor so that the units can germinate under the very broad range of environmental conditions that may follow the rains. If the first rainfalls are only light showers, leaching will be insufficient and the units will not germinate. This mechanism ensures that germination will take place only when sufficient rain has fallen not only to cause germination, but also to guarantee a certain degree of growth and development of the seedlings. This built-in gauge, together with loss of the dispersal units' viability, binds germination to the rainy season. The dispersal units collect mostly under the mother plant because of their weight. If the mother plant has been able to form

272 I The

Negev

a great number of them, mass germination occurs when rain is plentiful, but the chances of survival of the competing seedlings in the vicinity of the mother plant are poor. Since during a good rainy season, however, there are a number of floods, part of the dispersal units will be carried off into areas where the saltwort has not yet established itself and where there is no competition between seedlings. In this way new areas will be colonized by the species. On the other hand, if because of unfavorable conditions the mother plant has managed to ripen only a few dispersal units during its growing period, the chances of seedling survival in the vicinity of the mother plant are good even in drought years. The species in these years will not conquer new territories but will keep the original mother area occupied. We became acquainted with another adaptational mechanism of the biseasonal saltworts when observing seedlings that had germinated in the litter accumulated below a dead mother plant. In that particular year a first rain-inducing germination had been followed by a prolonged dry period, during which many seedlings dried out before their rootlets had reached the soil. These seedlings could become desiccated at any time up to 25 hours after the onset of imbibition and still be capable of being revived completely when water was again available to them. When drying out began 25-26 hours after the start of imbibition the seedlings did not recover. This "point of no return" is coincident with the beginning of radicle growth. In contrast to most higher plants, the germination of the saltworts starts not with the growth of the radicle but with the elongation of the seedling stem (hypocotyl) and the expansion of the cotyledons. The hypocotyl, like a lichen, is capable of desiccation as long as the rootlet does not grow. This property is most advantageous, especially at times when there is a long interval between the rains. Seedlings without this characteristic germinating above ground would die before the rootlets penetrate into the soil. Volken's saltwort (Salsola volkensii) developed another adaptational trait. It possesses two kinds of dispersal units, differing in color and germinability. One, like the dispersal unit of the unarmed saltwort, is green because its embryo contains chlorophyll and the other, for lack of it, is yellow. The germinability of the green dispersal units of Volken's saltwort and those of the unarmed saltwort is nearly identical, but the yellow dispersal units are dormant when freshly harvested and do not germinate even when all conditions for germination are favorable to them. They lose their dormancy slowly with time and subsequently remain germinable for long periods. Even after 5 years they can germinate fully under suitable conditions. The presence of two fruit types is of great ecological importance. Whenever it rains, one set of dispersal units germinates immediately after it is ripe, while the other remains ungerminated in the soil as a stock pile, germinating not earlier than a year after its formation. This behavior minimizes the threat to all annuals that in certain years soil-water

Adaptation

of Plants

to Desert

Conditions.

I | 273

conditions may be good at germination time, but drought may follow and prevent the seedlings from reaching maturity and completing their life cycle. In this way some seeds are left over in order to have a new try at germination at a later date when subsequent soil-moisture conditions may be more suitable for survival.

274 I The Negev

Fig. 170. A wadi of the Negev highlands in spring 1964.

XVII

Adaptation

of Plants to

Desert Conditions.

II

We dealt in the foregoing chapter with two types of xerophytes: plants that can suffer desiccation and plants that are active during the dry season. We shall now discuss the survival mechanisms of those desert plants that are active only as long as the upper soil layer is wet and become inactive during the dry season. (iii) Plants inactive during the dry season. When rainfall is plentiful these plants transform parts of the Negev and especially the wadis and depressions into desert meadows. This happened for instance in March-April of 1964, when soil moisture and climatic conditions were ideal for mass germination. The desert landscape was for a short time as undesertlike as possible (Fig. 170), with yellow, orange, blue, and violet winter annuals coloring the landscape. The slopes were dotted with the red-yellow flames of the desert tulip (Tulipa amplyophylla; Fig. 171a), the hillocks with the blue flowering stalks of ixiolirion (Ixiolirion montanum), while some of the fields were covered with the violet-black flowers of the Negev iris (Iris atrofusca; Fig. 171b) and in the wadis and foothills the enormous green leaves of the desert rhubard (Rheum palaestinum; Fig. 171c) were abundant. This rich flowering of 1964 resulted not only from plentiful rain but also from an advantageous distribution of precipitation when seasonal temperatures were suited to germination of many plant species. The colorful scene, however, was very short-lived; it was over after about 6 weeks. By the end of April the greenery had dried out and the Negev had returned to its normal gray, beige, and brown. In other years, especially in the drought year of 1962, one had to search very carefully to find even a single plant of one of these species that had flowered so abundantly in wetter rainfall years. In years with average rainfalls these plants appear and flower only in relatively small numbers when they can synchronize their active period with the soil-moisture conditions. At the beginning of the dry summer they either die or lose their green active parts above ground. There are three main groups of these summer-inactive xerophytes: plants with bulbs or rhizomes (geophytes, cryptophytes), diminutive perennial herbs (nanochamaephytes, hemicryptophytes), and winter annuals. The bulbs or rhizomes of the geophytes which are buried in the soil remain dormant during the dry season, well protected by layers of dead tissue or cork against drying out and overheating. When in this inactive state they need very little water, if any, to remain alive and so evade the drought conditions of the environment. The dormant bulbils of the Sinai blue grass (Poa sinaica), for example, can be heated to 80°C without any damage. However, shortly after the first rains and as soon as the soil is wet in the vicinity of the bulbs or rhizomes, they form with incredible speed roots and rootlets. Less than 12 hours after the first rain had wetted the upper 2 centimeters of soil the first rootlets appeared on the short-styled sedge (Carex pachystilis, Fig. 172) and a few hours

Adaptation

of Plants

to Desert

C o n d i t i o n s . II | 277

Fig. 171. (a) Desert tulip (Tulipa amplyophylla); (b) Negev iris (Iris atrofusca); (c) desert r h u b a r b (Rheum palaestinum).

278 I The N e g e v

Fig. 172. Short-styled sedge (Carex

pachystilis).

Adaptation

of Plants to Desert Conditions.

II | 279

later their dense network enmeshed the upper soil layer. The roots of many geophytes are very superficial. For example, the rooting horizon of the Sinai blue grass and of the short-styled sedge is never deeper than the upper 5-10 centimeters of the soil. Even the roots of the plants with large bulbs or rhizomes, like the Negev tulip and the desert rhubarb, do not penetrate layers deeper than 30-40 centimeters. Once root formation has started, the shoot apices situated inside the bulbs or on the rhizomes, well protected by layers of dry scales, become active and now form leaves above the ground. The leaves produce enough organic matter to permit either the bulbs to grow and form new bulblets or the rhizomes to elongate and develop new growing points. After some time the plants flower, producing fruits and seeds. During their activity, they use the available water freely, at a relatively even rate with little or no reduction of the transpirational surface. However, the moment soil moisture in the rooting horizon becomes scarce, the leaves immediately dry out and die, the rootlets disappear, and the bulbs and rhizomes become dormant again (Fig. 173). The dry year 1963 taught us some interesting facts about the geophytes of our Negev. The meager rainfall of the winter season 1962-63 wetted only the very uppermost few centimeters of the soil. The shallow-rooted blue grass and the sedge had just enough water to develop short-lived leaves but could not flower (Fig. 173e). We looked in vain for the deeper-rooting star of Bethlehem (Ornithogalum trichophyllum; Fig. 173d) and the Negev tulip. We searched for the desert rhubarb at exactly the same place where a year previously its large green leaves had been a prominent feature of the landscape, but we could not find even a single plant. We thought at first that the rhizomes had died; digging them out and studying them showed us that they were alive but dormant. One year later, when rainfall was more abundant, the same plants Fig. 173. Phenology of some desert plants: top, rainfall (mm); (a) una r m e d saltwort ( S a l s o l a inermis); (b) hairy storksbill ( E r o d i u m furtum); (c) H a n b u r y ' s squill (Scilla hanburyi); (d) thread-leaved star of Bethlehem ( O r n i t h o g a l u m trichophyllum); (e) Sinai bluegrass ( P o a sinaica); (/) short-styled sedge ( C a r e x pachystilis); hatching, plants with leaves; crosshatching, plants flowering and fruiting; stippiing, plants dormant or dead (in the case of the saltwort). Vertical black bars in (a) indicate the beginning of stem elongation.

280 I The

Fig. 174. A plant of the short-styled sedge (Carex pachystilis) a few days after the first rain. The leaves carry last year's dead tissue on top.

Negev

became active again and appeared in profusion. The adaptation of these geophytes to their environment is due to their ability to be active only when the environment is favorable and to remain dormant but nevertheless viable for long periods when conditions are not auspicious for their growth. Their speed of reactivation and high rate of activity during the short time water is available to their roots is another adaptational characteristic that enables them to complete their life cycle in the very short period available to them. Two geophytes need special mention, one because its adaptation to the desert environment is unique in some respects among the Negev xerophytes, and the other because its behavior is an ecological riddle—its developmental cycle seems to be out of harmony with the seasonal cycle of its environment. The shortstyled sedge covers large areas in loessial depressions. It is the first geophyte to sprout after a rain (Fig. 172), giving the bare Negev landscape its first light-green tinge. The speed of its emergence is due to the fact that its rhizomes do not have to form new leaves after the first rain. Although the upper parts of the leaves have dried out during the previous dry season, the base of the leaves stays alive. This basal zone, situated in the upper few millimeters of the soil, remains dormant during the dry season, protected by many layers of older dead leaves of previous years. A few hours after the first rain, the cells of the leaf base start to grow and elongate, pushing their upper dry parts above ground. The newly formed tissue becomes green. In this state the leaves look quite strange with their lower green parts bearing last year's dry brown tissues on top (Fig. 174). Only some time later are new leaves formed by the growing points of the buds. We found in the 1961 season that when there is too long an interval between the rains this process can be repeated by the same leaf during the growing season. Through this speedy reaction to the rains, the sedge is capable of using nearly every hour of the period when water is available for the production of organic material. Hanbury's squill (Scilla hanburyi) is a geophyte with two active periods during each year. The first growing period occurs at the end of the dry summer when the plant puts out its slender flowering stalks carrying small pale violet-rose flowers. No leaves appear at this time (Fig. 173c) and after seed formation the plant returns to dormancy. The second active period starts after the first rain and now only leaves are formed. The plant does not flower and the leaves dry out and die in February-March (Fig. 173c). At least two other Negev geophytes behave similarly, Urginea undulata and Pancratium sickenbergi. The behavior of the diminutive perennial herbs is best demonstrated by the hairy storksbill (Erodium hirtum). This plant is a small summer-inactive dwarf herb with comparatively large dissected leaves and big violet-lilac flowers which in their profusion contribute much to the blazing colors of the slopes whenever the desert blooms. The woody stems are very small and grow close to the ground. Their annual permanent increment in length and

Adaptation

of Plants to Desert Conditions. II | 281

thickness is insignificant and the stem of a plant tens of years old is still very small. They carry renewal buds which develop leafand flower-carrying shoots (Fig. 173b) after the first rains; these shoots are shed at the beginning of the dry season. Only the leafless woody stems, which can hardly be seen by the naked eye, remain to survive the summer in the dormant state. The main roots of the hairy storksbill penetrate more than 40-50 centimeters into the soil, exploiting a relatively large soil volume for water. Some of the roots develop fleshy tubers containing a large percentage of water and sugar, which have become a favorite food of the Bedouins. Many other Negev plants, such as the gray-leaved storksbill (Erodium glaucophyllum), the rupture wort ( H e m i a r i a hemistemon), and the desert mignonette ( R e s e d a muricata), belong to this same group of diminutive dwarf herbs. The water economy of the storksbill and the desert mignonette is typical of all hemicryptophytes, and, with one most important exception, is also similar to that of the summer-active rue and heliotrope. The transpiration rate of the leaves during the rainy season is high, but once the soil starts to dry out the transpiring surface is much reduced (Table 34). The plants can tolerate a relatively high saturation deficit (Table 35) before they gradually lose their leaves and become dormant. When the hemicryptophytes are no longer capable of supplying their daily increasing water deficits, they shed all their shoots. The duration of their active period is a function of the varying moisture conditions of their habitat (Fig. 173b). In relatively good years it may last for 4 months, whereas in dry years it may be restricted to 5 or 6 weeks. In a restricted active period only very few leaves are formed, and flowering is often suppressed. The winter annuals whose life cycle is restricted to the rainy season are the third group of desert plants inactive during the dry summer season. In the Mediterranean region of Israel only 28 percent of the plant species are winter annuals, whereas they represent 59 percent in the Negev. In even more extreme deserts, such as certain parts of the Sahara which may experience complete droughts for a number of consecutive years, the percentage is even higher and these plants may be the only ones to appear after the rare rainfalls. Shrubs, dwarf shrubs, trees, geophytes, and hemicryptophytes, on the other hand, are rarely found in the extreme deserts—an indication that the winter annuals are particularly well adapted to desert conditions. Their adaptational mechanisms differ in many respects from those described for other xerophytes. Their roots are mostly shallow (Fig. 175) and restricted in extent; they reduce their transpiration rate very little (Table 34) because they cannot diminish their transpiring surface to any effective degree; and in the majority of cases they do not tolerate large water deficits. But they possess the remarkable ability of being able to regulate their total body size according to the water conditions of their habitat. The rose of Jericho (Anastatica hierochuntica), for instance, when growing in extremely dry localities, is a tiny pigmy a few millimeters high with

282 I The Negev two or three branches, a few small leaves, and one to five fruits (Fig. 176). Where soil moisture is plentiful the plants reach 15-20 centimeters in height, attain a diameter of 25-30 centimeters, possess tens of branches, and have hundreds of fruits. The variable body size is also a measure of the great variability of developmental speed of the winter annuals, since the small individual plants go through their full life cycle in a much shorter time than the large ones. This is an important factor in their survival because in a habitat where water is scarce the time of optimal conditions is much shorter than in a well-watered one. Other adaptational traits of the winter annuals are their mechanisms for germination and seed dispersal, which enable their dispersal units either to lie dormant for long periods in the ground as a reserve when conditions are unfavorable for germination or enable them to germinate rapidly when the environment is favorable. This important trait led us to study particularly the physiology and ecology of germination of desert winter annuals. We give here only two typical examples, Gymnarrhena and the winged thorny spike (Pteranthus). Gymnarrhena micrantha is a dwarf composite which grows on regoid and hamadoid slopes, marly soils, loessial plains, and the like. After germination it forms a leaf rosette (Fig. 177), in the midst of which an inconspicuous, compressed stem carries a great number of densely packed flower heads (inflorescences). When a well-developed plant is dissected lengthwise, two kinds of inflorescences become apparent—numerous aerial flower heads visible above ground, as in Fig. 177, and a few subterranean ones borne in leaf axils 10-15 millimeters below the soil surface. The ovaries of the aerial flowers form small fruits, each of which carries at its apex a crown of fine hairs (pappus; Fig. 178b). The subterranean fruits are much larger and lack a pappus or carry

Fig. 175. Schematic drawing of the root systems of some winter annuals: (a) annual toadflax (Linaria haeJava); (b) desert mustard (Erucaria boveana); (c) Spanish aizoon (Aizoon hispanicum); abscissa, depth below surface (cm).

a

b

c

Adaptation

of Plants

to Desert

Conditions.

Fig. 176. The rose of Jericho (Anastatica hierochuntica): watered locality; (b) plant of very dry habitat.

II | 283

(a) plant of a

284

I The

Negev

Fig. 1 7 7 . G y m n a r r h e n a m i c r a n t h a ; t h e a e r i a l

flower

heads are clearly

visible.

Fig. 178. (a) Aerial seedling and (b) aerial fruit of Gymnarrhena micrantha; (c, d) their subterranean equivalents; the two seedlings are of the same age.

m

..

iSâi ^Ä'W·«»^- ' V"*'

j p T í t ' V f*

*»•> ™

Adaptation

of Plants

to Desert

Conditions.

II | 2 8 5

Fig. 179. Two subterranean fruits of Gymnarrhena micrantha germinating out of the dead mother plant. (By courtesy of D. Koller.)

286 I The Negev only a rudimentary one (Fig. 178d). At the beginning of summer the mother plant dies but the subterranean fruits remain attached to it. Before death the main root and the stem become lignified and hard—a state in which they can remain for years—while the dead, wirelike root continues to anchor the dead plant firmly in the soil. The subterranean fruits germinate out of their dead mother plant (Fig. 179). Where this happens year after year, one finds plants in which many generations have stayed together in one bunch with each successive generation germinating out of its preceding mother plant. The aerial fruits behave quite differently. When the dead receptacles bearing the aerial fruits undergo repeated cycles of wetting (by dew or rain) and drying, the fruits are detached from the receptacles through a complicated mechanism. The light free fruits, which carry a pappus that functions like a parachute, are easily dispersed by the wind. Gymnarrhena resembles Volken's saltwort in that the same mother plant forms two kinds of fruits. In the case of Gymnarrhena they differ in size, position on the mother plant, morphology, and biological function (amphicarpy). The subterranean fruits, which cannot be dispersed, are really "antidispersal units," whereas the aerial fruits are true dispersal units. But this is not the only difference of the two fruit types. When both are germinated under the same conditions they produce two kinds of seedlings, differing in anatomical structure, size, and growth rate (Fig. 178a, c). The subterranean seedlings are much larger, thicker, and heavier than the aerial ones. Laboratory experiments prove that they are also more drought-resistant and drought-tolerant, surviving water stresses that kill the whole population of the aerial seedlings (Tables 36 and 37). Our observations in the field confirm

Table 36. Mortality of seedlings (percent dying) of G y m n a r r h e n a m i c r a n t h a grown in containers f r o m w h i c h w a t e r w a s withheld for various periods. Days without water Seedlings Aerial Subterranean

1

3

5

7

29 0

71

87 0

100 37

0

Source: Koller and Roth, modified.

Table 37. Mortality of seedlings (percent dying) of Gymnarrhena micrantha w h e n the w a t e r content of the soil w a s kept at different levels. Water content of soil (ml/400 gm) Seedlings

60

45

25

20

Aerial Subterranean

12 0

40 0

42 8

54 11

Source.· Koller and Roth, modified.

Adaptation of Plants to Desert Conditions. II | 287 this laboratory finding. The aerial fruits, which are blown off by the wind, germinate wherever their dispersal is arrested by an obstacle. In years with little rain, many and sometimes all of them die, whereas most of the subterranean seedlings survive. Even in years with abundant rain the mortality rate of the aerial seedlings is relatively high. Moreover, water stress affects the formation of aerial and subterranean flower heads and fruits. In bad years only the subterraneans are produced by the plant. The two fruit types differ also in their germination requirements, especially their sensitivity to light and heat (Fig. 180). The amphicarpy of Gymnarrhena has interesting ecological consequences. The subterranean fruits ensure survival of the species because they are formed even w h e n water conditions are unfavorable and because they germinate in a locality where the mother plant has succeeded in completing its life cycle. The chances are good, therefore, that the next generation developing from subterranean fruits will be equally successful in the mother locality. Germination out of the mother plant has an additional advantage: the roots of the mother plant shrink when drying and form capillaries in the soil which after a rain rapidly fill with water. The dry, dead tissues take it up, swell, and retain it for some time, thereby improving the conditions for the new generation. Germination below ground is another advantage in guaranteeing readier access to soil water and protection against evaporation.

Fig. 180. Germination percentages of aerial and subterranean fruits of G y m n a r r h e n a micrantha at different temperatures (5-25 C°) in light and in darkness: open circles, aerial fruits in light; solid circles, aerial fruits in darkness; open triangles, subterranean fruits in light; solid triangles, subterranean fruits in darkness. (After Koller and Roth.) %

germ".

80 60

40

20

\

0

0

5

10

15

20

\ 25 30 TEM P. °C

288 I The Negev

Fig. 181. The winged thorny spike (Pteranthus dichotomus), bearing many dispersal units.

Adaptation

of Plants to Desert Conditions. II | 289

T h e biological function of the aerial fruits, which formed only in good years is to occupy by dispersal new territories for the species. Their small size, low weight, and possession of a pappus adapt them well to fulfill this function. Theirs is a trial that will succeed only in years with favorable soil-moisture and germination conditions. But even in good years seedlings developing from aerial fruits can establish themselves only in favorable localities— beneath stones in depressions, fissures, and cavities where runoff water has collected—since they germinate above ground and cannot tolerate drying. If they succeed here then they will produce a n e w generation which in turn will develop subterranean fruits. In this w a y a new promising habitat will be conquered for the species. T h e winged thorny spike (Pteranthus dichotomus; Fig. 181) belongs to the pink family and is endemic to the Saharo-Arabian region. The dispersal unit has a flat stalk with a compacted fruiting head containing a number of fruits (Fig. 182). T h e fruiting heads develop from inflorescences carrying spiny branches, each one crowned by a single flower. W h e n fully developed, and depending on the sequence of development of the branches, each inflorescence has one flower of the first, two of the second, and four of the third order (Fig. 183). E a c h flower then forms a one-seeded fruit which remains surrounded by four spiny leaves making up a pseudocarp (Fig. 182). Theoretically, therefore, each dispersal unit can carry a m a x i m u m of seven pseudocarps, each containing a single one-seeded fruit. But most units do not bear their full complement and in the extreme case they contain only one firstorder pseudocarp. T h e mature dispersal units fall off the dead mother plant, but because of their compact structures, spines, ánd weight they remain nearby. Of 464 dispersal units we studied, which had germinated in a typical habitat of the winged thorny spike, 85.6 percent had developed only one seedling, 14.4 percent two, and in no case did we observe more than two seedlings per unit, although a dispersal unit contains 1 - 7 seeds capable of germination. As in the case of the unarmed saltwort, with its internal "rain gauge," the explanation lies in the presence of a substance that inhibits germination and requires partial leaching before germination starts. W h e n we dug seedlings out from the soil and counted the emergence from 464 dispersal units, we made a puzzling observation. All the seeds of those dispersal units that carried exclusively first-order pseudocarps (8 percent of the total number) had germinated. Of the remaining 92 percent of the units that carried pseudocarps of the first and higher orders, only seeds of second- and of third-order pseudocarps had germinated, while the seeds of the first-order pseudocarps remained ungerminated. Laboratory experiments gave us the key to this unexpected behavior. We arranged the dispersal units in our possession into three groups. T h e first was composed of units that had formed only first-order pseudocarps (I), the second contained orders I and II, and the third, all three orders (I, II, III). We took the pseudocarps off and put

—--^J I

b

c

I

_J

d

Fig. 182. Winged thorny spike (Pteranthus dichotomus): (a) dispersal unit carrying on its stalk st spiny branches br bearing pseudocarps ps (after Zohary, Flora Paiaestina); (b) pseudocarps containing a one-seeded fruit fr; (c) fruit with seed s surrounded by fruit coat co; (d) seed; the black spot on the seed is the scar of the funiculus, that is, the short stalk that connected the ovule to the ovary.

290

Fig. 183. Schematic drawing of a dispersal unit of the winged thorny spike (Pieranthus dichotomus) showing the arrangement of the pseudocarp of the first (I), second (II), and third (III) orders; st, stalk; br, branch; ps, pseudocarp.

I The Negev

them to germinate separately. The first-order pseudocarps did not germinate at all when taken from dispersal units that carried all three orders. But a high percentage of first-order pseudocarps derived from units containing only first-order pseudocarps germinated. The germination of the same pseudocarps taken from units with two orders had a lower percentage of germination. The germinability of pseudocarps of one order of a dispersal unit is therefore determined by the presence or absence of pseudocarps of the other orders—a factor of ecological importance, as will now be explained. The three orders of one dispersal unit do not develop at the same time. Order I is the first to be formed, then order II, and lastly order III. In drought years water stress forces the plants to restrict their development, as with all xerophytes. In such years the winged thorny spike does not succeed in forming all three orders of pseudocarps and consequently the number of dispersal units carrying only first-order pseudocarps will be much greater than in good years, when most dispersal units will develop two or three orders of pseudocarps. Consequently, after a drought year the majority of the first-order pseudocarps will be able to germinate easily during the next rainy season. After a good year most dispersal units carry three sets of pseudocarps: those that germinate readily, those that will not germinate the next year but are viable, and those that are intermediate. Thus a reserve of viable seeds will always remain in the soil. But this is only part of the story. When the germination of pseudocarps, fruits, and seeds of the various orders was tested under various controlled conditions of temperature and light, we found that each of these units has different germination requirements (Table 38). Thus a dispersal unit carrying all three orders of pseudocarps contains a combination of units each of which has different requirements for germination and responds differently to light and temperature. This quite complicated case of the winged thorny spike deserves particular description because, together with that of Gymnarrhena, it is an excellent demonstration of the manner in which T a b l e 38. G e r m i n a t i o n ( p e r c e n t ) of fruits of the w i n g e d t h o r n y spike ( P t e r a n t h u s dichotomus) w i t h different o r d e r s of p s e u d o c a r p s , at different t e m p e r a t u r e s in light a n d in d a r k n e s s . Order of pseudocarps II

8 15 26 30 35 37

III

Light

Dark

Light

Dark

Light

Dark

18 50 65 72 12 0

12 23 8 16 4 0

72 89 97 97 66 65

58 83 90 84 20 24

90 98 100 100 100 91

99 97 95 96 89 82

Adaptation

of Plants to Desert Conditions.

II | 291

winter annuals have developed an answer to the challenge of the desert. For them, much more than for the perennials, the main danger lies in the enormous variability of the environmental conditions from year to year and also from habitat to habitat. They counteract this by being endowed with an even greater variety and variability of morphological, developmental, and physiological responses, which provide an ever-present reserve of viable seeds lying dormant in the soil, ready for all probable climatic eventualities. Another adaptation characteristic of the winter annuals is the dispersal of their seeds. Two examples will suffice to illustrate the process: the buck's horn plantain or buckhorn (Plantago coronopus) and the dwarf oxeye (Asteriscus pygmaeus). The buck's horn plantain grows abundantly on loessial plains of the Negev highlands. When flowering, it develops a number of erect stalks carrying at their apexes cylindrical flower heads. The fruit is a capsule surrounded by small leaves, which when dry envelop it completely. After formation of fruit the plants dry out and die, and the stalks bend until they touch the ground (Fig. 184a). During summer the indehiscent capsule remains attached to its stalk and does not release its seeds. When a little water is poured over the dry plant, the stalks after a few minutes curve upward (Fig. 184b) until they are erect. At the same time the leaves enclosing the fruit capsule move outward, exposing it completely. Some of the capsules fall off, releasing their seeds. This little experiment simulating a rainfall shows that seed dispersal happens only after the rainy season has started. Germination harmonizes with the timing of dispersal. We removed seeds from their capsules at their maturity (mostly in May) and tried to induce germination under supposedly suitable conditions. We found that the seeds took up water, but did not germinate in light, in darkness, or under a temperature range of 10°-25°C. However, if these seeds were stored for 5-7 months or, in the field, were removed from their capsules at the beginning of the rainy season, they germinated under the same conditions that had previously failed to induce germination. The seeds therefore have afterripened, that is, they have become germinable. In nature afterrippening takes place during the dry summer, when the seeds could not germinate anyway for lack of water. The length of the summer is just enough to bring the afterripening process to its final stage—another example of the perfect adaptation of desert plants to the "time structure of their environment." The dwarf oxeye has leaf rosettes with flower heads emerging from their centers (Fig. 185a). The flower heads are surrounded by a crown of bracts (involucral leaves). When the plants dry out, the lower lignified portions of the bracts curve inward and completely cover the fruiting heads containing the fruits formed by the flowers (Fig. 185b). If moistened by water or water vapor the bracts curve outward (Fig. 185c) and some peripheral fruits are set free and dispersed by rain or runoff, while those in the center remain attached to the fruiting head. In contrast to Gymnarrhena,

292

I The Negev

Fig. 184. (a) A dry, dead plant of the buck's horn plantain (Plantago coronopus) with fruit stalks; (b) the same plant a few minutes after water has been poured over it; the stalks have curved upward.

Adaptation

of P l a n t s to Desert

C o n d i t i o n s . II | 293

Fig. 185. Dwarf oxeye (Asteriscus pygmaeus): (a) flowering plants; (b) dry fruiting heads (left of potherd); (c) the same fruiting heads a few minutes after water has been poured over them.

294

I The Negev

germination never takes place while the fruits are attached to the mother plant, and only dispersed fruits can germinate. W h e n the rain has stopped, the bracts again curve inward to close over the remaining fruits. This cycle is repeated with each subsequent rain until all the detachable fruits have been set free. Complete dispersal of all the fruits of one plant m a y on rare occasions be accomplished in a n u m b e r of cycles in a very rainy year or it m a y carry through several dry years. We have observed individual dry plants that even after 5 years still possessed undispersed germinable central fruits. Since the fruits remaining attached to their h e a d s are liberated only by water in its liquid state, the high survival value of this "fractionated" dispersal is evident. The last part of this chapter will deal with an interesting and complicated problem posed by desert plants, which also is a problem with a long history. In 1884 a young German botanist, Dr. Georg Volkens, traveled to the Egyptian-Arabian desert to investigate the relation between the anatomical structure and the physiological function of plants, w h i c h he believed would be more obvious in the desert than elsewhere because of the overriding importance of water in the desert. In 1887 he published his observations and described certain anatomical structures of desert plants which in his opinion these plants had developed as f u n c tional adaptations to desert conditions. Since that time the discussion on the problem of the functional value of the anatomical structure of desert plants has continued unabated. Are there anatomical structures specific to desert plants? W h a t is their ecological value, if any? How are they related to the desert environment? Even today, we have no clear-cut answers to these questions. We shall, however, restrict our discussion to the transpiring and photosynthesizing organs of xerophytes, since we k n o w most about the anatomy of these plant parts. The basic structure of the transpiring and photosynthesizing organs of the desert plants, that is, leaves and, for some plants, stems, reveals five basic types; as usual, there are also transitions b e t w e e n types. (i) S c l e r o m o r p h o u s 1 stems and leaves. These are characterized by the presence of tissues (sclerenchyma) composed of thickwalled cells that give the organs mechanical strength. They are also characterized by very thick cuticles and outer walls of the epidermal cells, by sunken stornata, and sometimes by an epidermis consisting of more than one layer of cells. Very often the cells, especially those carrying out photosynthesis, are smaller than normal. The best examples of scleromorphy are the photosynthesizing leafless stems (Figs. 186 and 187), w h i c h are all built along the same lines, irrespective of w h i c h families the plants m a y belong to. They include b u c k w h e a t (Calligonum comosum; Fig. 187/), soup h e r b 2 (Pituranthos tortuosa; Fig. 187c), desert lavender 1

The term is derived from the Greek word sklëros hard and morphe form. We intentionally do not use the more usual term "xeromorphous" because it indicates a relation between structure and dry (xeric) habitat. 2 We called this plant "soup herb" because it tastes like a concentrated soup extract.

Adaptation

of Plants

to Desert Conditions.

II | 295

Fig. 186. (a) Schematic diagram of a cross section of the stem of the white desert broom (Retama raetam); (b) enlargement of the area indicated by the circle in (a); (c) enlargement of the area indicated by the circle in (b), showing a stoma; (d) schematic diagram of a cross section of the stem of the shrubby horsetail (Ephedra alte); (e, f) enlargements of the area indicated by the circle in (d); (g) schematic diagram of a cross section through the flowering stalk of the annual toadflax (Linaria haeiava); (h) enlargement of the area indicated by the circle in (g). In (a), (d), and (g) stippling indicates vascular bundles; hatching, green photosynthesizing tissue; crosshatching, mechanical tissue; blank area, tissue consisting of nongreen, thin-walled cells (parenchyma); the outermost layer is the epidermis. In the detailed drawings, stippling indicates intercellular spaces; thick black lines, cuticle; ep, epidermis; m, mechanical tissue; ph, green photosynthesizing cells.

296 I The Negev (Lavandula coronopifolia; Fig. 187e), gnetum (shrubby horsetail, Ephedra alte; Fig. 186d), desert asparagus (Asparagus stipularis; Fig. 187a), berry mignonette (Ochradenus baccatus; Fig. 187b), spiny zilla (Zilla spinosa; Fig. 187d), and white desert broom (Retama raetam; Fig. 186α). This near uniformity of anatomical structure is hardly strange, since most plant stems are constitutionally scleromorphous, irrespective of any photosynthesizing functions. Whereas leaves are characterized by great structural variety, stems follow basically similar structural plans. The specific anatomical mark of the photosynthesizing stems is the presence of green tissues at their periphery. In this respect only small structural differences exist between the photosynthesizing stems of leafless summer-active perennials and those of leaf-bearing winter annuals, whose stems and flower-bearing stalks are also mostly green and participate in photosynthesis; see, as one of many examples, Fig. 186g depicting the stem of the annual toadflax, Linaria haelava.

Fig. 187. Schematic diagrams of cross sections of various stems: (a) desert asparagus (Asparagus stipularis); (b) berry mignonette (Ochradenus baccatus); (c) soup herb (Pituranihos tortuosa); (d) spiny zilla (Zilla spinosa); (e) desert lavender (Lavendula coronopi/olia); (/) buckw h e a t (Calligonum comosum); symbols as in Fig. 186. In (b) and (d) the vascular bundles are located in the strongly developed ring of mechanical tissue.

Adaptation

of Plants to Desert Conditions.

II | 297

Fully scleromorphous leaves, not very common in desert plants, are mainly restricted to thistles and prickly thistlelike plants, or to the members of two families, the grasses and the sedges (see Fig. 188, Sinai bluegrass, Poa sinaica). In these plants scleromorphy is a typical constitutional feature, not dependent on their habitat.

α ep

ph

Fig. 188. (a) Schematic diagram of a cross section of a leaf of the Sinai bluegrass (Poa sinaica); (b, c) a stoma and enlarged details of the area indicated by a circle in (a); symbols as in Fig. 186.

(ii) Malacomorphous 3 leaves. By far the majority of desert plants, annuals and perennials, summer active and inactive alike, have leaves that do not carry a single scleromorphous feature. They are characterized by thin cuticles and outer cell walls of the epidermis. Furthermore, the stornata lie in the epidermal plane, have large cells, and possess no special mechanical tissues. Figures 189 and 190 show such an anatomical leaf structure, typical of a number of desert plants belonging to various families. Certain common characteristics are best explained by a comparison of their structure to that of the malacomorphous leaf of the Judas tree (Cercis siliquastrum; Fig. 189a), a common Mediterranean species. It is dorsiventral, that is, the anatomy of its upper side differs most distinctly from that of the lower. The upper part of the leaf tissue is composed of cells ("palisades") perpendicular to the leaf's surface containing many green chloroplasts, whose main function is photosynthesis. The tissue of the lower side of 3

From Greek malakos soft and morphe form.

298

I The

Negev

the leaf is made up of smaller rounder cells ("spongy tissue") between which are large spaces ("intercellulars") containing air. Stornata are found only in the lower epidermis and are missing completely in the upper. The anatomical structure of the malacomorphous leaves of desert plants is generally very different. With very few exceptions they are not dorsiventral and possess stornata on both sides—a feature common to the leaves of all desert plants, including the scleromorphous and succulent ones. In many cases, especially in annuals, the leaf tissues consist of more or less round undifferentiated, isodiametrical cells; an example is the Egyptian marigold (Calendula aegyptiaca; Fig. 189b). In others it is made up of palisade cells only, as in the diandrous rupture wort, Hemiaria hemistemon; Fig. 190), the sagebrush (Artemisia herba alba; Fig. 152), and the Egyptian woundwort (Stachys aegyptiaca; Fig. 189d), or of palisades on both sides of the leaf with a kind of spongy tissue in the middle, as in the desert mignonette (Reseda muricata; Fig. 189c). There are all kinds of transitional types among those mentioned, but one outstanding feature is common to all: with the exception of the epidermis, the connection between the cells of the leaf tissue is loose; the cells just touch each other and the intercellular spaces are very large. In many cases the cells are so slightly connected that on occasion when we prepared transverse sections in order to study the leaf anatomy under the microscope we found to our astonishment that the isolated cells fell out. Even the photosynthesizing tissue of some scleromorphous stems is similar, as for example in the desert toadflax Fig. 189. Diagrams of cross sections of various leaves: (a) Judas tree (Cercis siliquastrum); (b) Egyptian marigold (Calendula aegyptiaca); (c) desert mignonette (Reseda mur ¡cata); (d) Egyptian woundwort (Stachys aegyptiaca); (e) Roth's garlic (Allium rothii); ( f ) Negev tulip (Tulipa amplyophylla); stippling indicates intercellular spaces.

IOOJJ

Adaptation

of Plants to Desert Conditions.

II | 299

(Linaria haelava; Fig. 186g). The short-lived leaves of the summer-active plants with photosynthesizing stems are also malacomorphous.

Fig. 190. (a) Schematic diagram of a cross section of the leaves of the rupture wort (Hemiaria hemistemon); (b, c) enlargements of areas indicated by the upper and lower circles, respectively, in (a).

(iii) EnchyJomorphous 4 (succulent) leaves. The leaf of the bean caper (Zygophyllum dumosum; Fig. 191) is a good example of leaf succulence. It contains a great amount of water stored in the large cells of the centrally located storage tissue and it is surrounded on all sides by much smaller green photosynthesizing cells. There is no dividing line between the two tissues. In other succulent leaves, such as Forskahl's marigold (Mesembryanthemum forskahlei), the two tissues are sharply separated. The typical succulent leaf has none of the scleromorphous characters, its cuticle and outer epidermal cell walls are especially thin, and the nunjber of stornata per unit surface is small. It is either cylindrical or flat but very thick. In both cases the ratio of external leaf surface to volume is small. Since the great majority of leaves of desert plants have a slight tendency to succulence, this is true of all types to some degree. (iv) Leaves with malacomorphous tissue covered by a scleromorphous epidermis. Such leaves seem to be a constitutional feature of most of the plants belonging to the lily family. The leaf tissue is loose and of the same types as the purely malacomorphous leaves (Roth's garlic, Allium rothii; Fig. 189e). In some cases (Negev tulip, Tulipa amplyophylla; Fig. 189f) the cells are elongated and parallel to the leaf surface. The epidermis has thick cuticles and outer cell walls and sunken stornata. (ν) Stems and leaves with an enchylomorphous core and a scleromorphous epidermis. Such an arrangement is typical of the 4

From Greek enchyios succulent and morphe

form.

Fig. 191. (a) Schematic diagram of a leaf section of the bean caper (Zygophyllum dumosum); (b) enlarged details of the area indicated by a circle in (a).

300 I The

Negev

photosynthesizing stems of many members of the goosefoot family (Fig. 149) and in some cases also of their leaves. The initially succulent petioles of the bean caper develop during summer a most scleromorphous epidermis (Fig. 154). These are the main data that can be observed in our Negev desert. What is their ecological significance? It seems to us that the one point with over-riding importance is the fact that, irrespective of the shape of the leaf, whether cylindrical, flat, or of an intermediate form, there is no leaf surface of any desert plant without stornata. The structure and position of the leaf tissues are such that wherever there are stornata there are cells capable of carrying out photosynthesis. This means that when water conditions permit, photosynthesis can be intense, enabling the desert plants to exploit efficiently the relatively short periods when water is available for production of organic materials. Even in those plants in which decreasing transpiring surface is a function of increasing drought, the same is true of the small surfaces remaining for photosynthesis. Since photosynthesis depends inter alia on the amount of carbon dioxide taken up through the surface of the photosynthesizing cells, and, because the photosynthesizing cells of leaf tissues of the majority of desert plants have a loose arrangement, the single cells have a large free surface which significantly intensifies the photosynthesis of each. One might argue that the structural features expediting photosynthesis at the same time increase water loss, but this would be true only for the time while the stornata are open and transpiration is really intense. The plants' countermeasures for reducing transpiration have already been pointed out. In all desert plants, with the exception of the pure succulents, the closure of the stornata is highly effective in cutting down water loss since cuticular transpiration is very low. The scleromorphous structure of the epidermis reduces cuticular transpiration. But since many plants with nonscleromorphous skins can reduce their cuticular transpiration as efficiently, it is apparently not only the thickness of the cuticle and of the outer cell walls of the epidermis that serves this purpose but also the submicroscopic structure and chemical composition of the cuticle. We know very little of these last-mentioned complicated factors and processes. Succulent leaves have a water reserve on which they can draw. The cell walls of their tissue are thin and elastic and can either shrink or expand according to their water content. Despite their water reserve and their low rate of transpiration, their faculty for limiting transpiration is low and, contrary to common opinion, they cannot be considered especially drought-resistant. This observation does not apply to plants like the cacti (not represented in the Negev flora), where the stem is succulent, contains an enormous amount of water, and is protected by a highly scleromorphous skin.

XVIII

Adaptation to Desert

of

Animals

Conditions

To most observers traveling through the Negev in the daytime the desert seems to be empty of animal life. The sudden appearance of any animal in the vast desert area, the desolate, dry, and sunscorched wilderness, therefore always evokes a feeling of amazement and wonder. The twitter of a well-camouflaged desert lark, heard but not seen from a stony slope on a hot midday, the swift movement of a lizard in a dry wadi bed that has not seen water for many months, a golden spiny mouse running to and fro among the rocks, or a black beetle moving about on the hot soil which one never dares to step on barefooted, a herd of gazelles, a lone camel wandering at a distance of tens of miles from any water source will impress any observer who realizes how puzzling and enigmatic the existence of animal life in the desert really is. This is no less true of the scientist who investigates animal life in the desert. The more he learns about it, the more he will marvel at the innumerable ways and means used by nature to enable animals to live in this extreme environment. Desert animals, like all living organisms, carry their heritage of aquatic origin within their physical composition. All the metabolic processes occurring within their bodies take place in an internal environment in which the presence of a minimal constant amount of water is an absolute necessity. Water constitutes 60-70 percent of the bodies of all animals, at least when in an active state. The maintenance of so great a water reservoir in the dry and hot desert atmosphere seemingly defies the laws of physics and constitutes the major problem of animal life in deserts.

Fig. 192. Main zoogeographical units of southern Europe, Middle East, a n d North Africa: black, Mediterranean region; slanted hatching, Irano-Turanian region; vertical hatching, S a h a r o - A r a b i a n region; light stippling, S u d a n i a n region; heavy stippling, Colchic region; crosshatching, Euro-Siberian region. (From Atias of Israel.)

302 I The Negev Taking into account the narrow range in which the body temperature of animals fluctuates—which is particularly limited in homeothermic animals (those that maintain a constant body temperature)—as compared with the extreme temperature fluctuations of the desert environment, it is obvious that the main arenas in which the adaptations of desert animals take place are water economy and heat balance. Additionally, the l o w productivity of the desert forces its animal inhabitants to increased activity in providing themselves with sufficient food and makes the water problem and heat burden even more acute. The geographic location of Israel at the meeting of three vast Zoogeographie units (Fig. 192) is the key to an understanding of the multitudinous forms of animal life in the Negev and the great variety of patterns of adaptation to desert conditions. The variegated topographic relief of the Negev of today, the climatic changes in times past, and the numerous varieties of rock formations create an abundance of biotopes, of different ecological niches, for animals of the most divergent ecological requirements. The density of different biotopes in the limited area of the Negev, which is the main factor in its wealth of biological phenomena, and even more the mobility of animals, make it difficult to delimit the zones of animal distribution. The botanists are in this respect in a much better position and have been able to divide the Negev into distinct phytogeographic regions (see Fig. 3) which are only partly congruent with the distribution zones of animals. The only outstanding geographic demarcation of animal distribution runs near the northern ridge of the Makhtesh Ramon, Table 39. Distributional patterns of vertebrates in the Negev, demonstrating the Zoogeographie significance of the " R a m o n - Z o h a r l i n e " (Fig. 3). A p p r o a c h i n g the line f r o m N . W .

Distributed S.E. f r o m the line Mammals

L o n g - e a r e d hedgehog + ( H e m i e c h i n u s

auritus)

G o l d e n spiny mouse + A c o m y s russatus

Garden doormouse + (Eliomys melanurus)

Bushy-tailed jird + S e k e e t a m y s

Palestine m o l e rat + ( S p a l a x ehrenbergi)

calurus

N u b i a n ibex + C a p r a nubiana

Tristram's jird + ( M e r i o n e s tristrami) Great E g y p t i a n gerbil + (Gerbilius p y r a m i d u m ) Birds Palestine bubbler + Turdoides s q u a m i c e p s W h i t e - r u m p e d w h e a t e a r + Oenanthe Desert partridge + A m m o p e r d i x L a p p e d - f a c e d vulture + A e g y p i u s

leucopyga heyé tracheliotus

Reptiles H a r d o u n lizard + ( A g a m a stellio)

Studner g e c k o + T r o p i o c o l o t e s studneri

Snake-eyed lizard + (Ophisops elegans)

E g y p t i a n d a b b lizard +

Fringed-toed l e o p a r d lizard + ( A c a n t h o d a c t y l u s pardaJis)

Sinai agama + A g a m a s i n a i t a

Striated desert l i z a r d + ( E r e m i a s Olivieri) Amphibians

Green toad + ( B u f f o

viridis)

Uromastix

aegyplius

Adaptation

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| 303

continuing northward to the Hatzera anticline and reaching the Zohar area to the north (see Fig. 3, line a-b); for simplicity's sake we shall call this boundary the "Ramon line." The distribution maps of certain animals illustrate this very clearly. Many animals that have a Mediterranean distribution pattern range from the northwest to this line, which also serves as a border for many semidesert animals. This boundary is even more evident when one observes the distribution of extreme desert animals living in the area southeast of this line (Table 39). What is true for the vertebrates is no less valid for many invertebrate animals. We take as an example the land snails. That land snails are present at all in a desert is invariably a source of great astonishment to the visiting tourist. Two species are especially noticeable. One is the desert snail (Eremina desertorum), which sometimes covers the tops of dwarf bushes in such density that the plants look as if they carried large white blossoms. Its habitat is sandy biotopes northwest of the Ramon line. The other species is the white desert snail (Sphincterochyla boissierii; Fig. 193), whose white shells cover loess soils and rocky slopes of the same area. Many other species of snails have the same distribution. There are very few land snails that penetrate the demarcation line southeastward, and even they disappear toward the Arava depression. It is most thrilling to see that the same biotope northwest and southeast of the boundary line is inhabited by different animals. A good example of this is seen beneath the stones of the desert pavement, which provide a good shelter for many animals and create one of the most densely populated animal biotopes in arid zones. The humidity preserved here, the low soil temperatures, and the protection from the intense solar radiation attract even animals normally averse to desert conditions. Northwest of our Fig. 193. The white desert snail (Sphincterochyla (Courtesy of Joseph Orr.)

boissierii)

mating.

304 I The Negev demarcation line this biotope is the classical habitat of spiders, centipedes, scorpions, solifuges, fishtails, beetles, and many other invertebrates. It is also a refuge for reptiles, especially snakes and lizards. But as with the land snails this association thins out steadily southeast of the line. In this vast wilderness one has to turn over dozens of stones in order to find a single scorpion, snake, or beetle, and a great number of species common to the northwest of the line are completely absent here. Sometimes just a few hundred meters separate the distribution area of a species on one side of the line from the distribution area of its ecological equivalent on the other side. This is true, for example, of the lizard agama. The common agama (Agama stelio) is very abundant northwest of the line, and the sinaitic agama (A. sinaita) lives in the same biotope southeast of the line. The Ramon line of Zoogeographie distribution is mainly a function of the climatic northwest-to-southeast gradient of Israel. This is one of the factors determining the nature of ecological associations. The other parameters involved are the local topographic relief and the edaphic (soil) conditions of the habitat. As mentioned already, there are sandy biotopes on both sides of the Ramon line. In the western Negev they are a northern extension of the vast sandy areas of northern Sinai, serving as an invasion route for many desert animals and plants that penetrate far northward into the Mediterranean zone of Israel. It is hardly accidental that the same passage, the "via maris," served the same purpose in the human history of the area. The psammophilic animals (that is, those that prefer sandy conditions) inhabiting this biotope form a very typical ecological association, conspicuous in its morphological and behavioral adaptations to the sandy and highly mobile substrate. The most noticeable adaptations for walking on loose sand are the palms of the gerbil, (Gerbillus), which are covered by a long hair tuft, the long fingers of the fringed-toed sand lizard (Acanthodactylus scutellatus; Fig. 194), the area of which is enlarged by thornlike scales, hairs, and bristles, the elongated leg segments (tarsi) of various beetles, and the like. Other animals of the same biotope capitalize on the ease with which one can dig oneself into the sand and disappear from the surface in a matter of a few seconds or minutes. How many soldiers of the British 8th Army (the "Desert Rats") and of the cohorts of Rommel (the "Desert Fox") saved their lives by using this feature of the sand! Typical animal sand burrowers and sand troglodytes are the skinks (for example, Scincus scincus), the sand snake (Lithorhynchus diadema), the highly poisonous pygmy sand viper (Aspis vipera; Fig. 195), and the scarbid beetle (Temnorrhynchus baal). A very different but well-defined psammophilic association lives in the sandy biotopes of the Arava depression, where desert conditions are much more extreme and which are geographically and zoogeographically related to the sandy areas of the southern Transjordanian desert. There species like the lesser Egyptian gerbil (Gerbillus gerbillus), the cerastes viper (Aspis cerastes), and

Adaptation

of Animals

to Desert

Conditions

Fig. 194. The fringed-toed sand lizard ( A c a n t h o d a c t y l u s (Courtesy of Joseph Orr.)

| 305

scutellatus).

306 I The Negev

Fig. 195. The pygmy sand viper (Aspis vipera) digging itself into sand. (Courtesy of Joseph Orr.)

Adaptation

of Animals

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the nocturnal Persian ground gecko (Stenodactylus doriae) show the same adaptations to their sandy environment described above. In the mountainous areas of the Negev the rocky relief, dissected by wadis, is the key to the division of the general landscape into a great number of different biotopes, such as hammadas, regs, hammadoid slopes dipping at different angles to the level of the wadis, wadi terraces and floodplains covered by loess, cliffs, and canyons, to cite only a few. Each of these constituents of the general landscape appears as a defined biotope. Unfortunately we still lack any microclimatic research on the microenvironment of these biotopes, a study that would permit us to understand much better the way of life of various animal associations typical of each biotope. The adaptations of animals to their desert environment are manifold. We shall deal first with the domesticated animals of the Bedouins. A Bedouin's life in the desert would be impossible without his camels, sheep, goats, and donkeys. They are his livelihood and maintain him and themselves in the desert, to which they are especially adapted although they all are domesticated animals. (i) The camel. The exceptional ability of the camel to withstand desert conditions is known to everybody. Since Biblical times the camel has been associated with the desert of our area, the Semitic peoples, and nomads. It is cited 52 times in the Bible; the book of Genesis alone, telling the story of the origin of the Jewish people, mentions it 24 times and the word for camel in all Western languages is derived from its Semitic name (in Hebrew "gamal"). The camel is the source of innumerable stories and legends in the folklore of all civilizations that ever thrived in the Negev. Ever since its domestication, a few thousand years ago, the camel has accompanied the nomad in the desert and fulfilled the task of an animal of burden and work. Its milk (up to 10 liters a day) is used for making cheese, and the high-quality wool (about 3 kilograms from each animal) for weaving. The camel has also provided meat for the population of towns bordering on deserts. Through the influence of modern civilization the number of camels is decreasing rapidly, along with the population of its present-day masters, the Bedouins. In certain areas camels have even disappeared completely. In an official census made in 1943, 30,000 camels were counted in the Negev; today that figure has dwindled to a mere few thousand. Here and there in the Negev one can still see them plowing the fields of the Bedouins (Fig. 1), though the tractor has mostly replaced them. In the central and southern Negev one may meet them, even today, wandering freely in herds, grazing in the wadi beds without any owner to watch over them. Only once every 5 to 7 days in the summer, and 20 to 30 days in the winter, do their owners come to give them some water. They can be found in the remotest and most desolate areas of the Negev, even in the middle of the hottest of summer days, exposing their bodies without any mercy to the fierceness of the desert climate. The mystery of their survival in the desert is fully

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demonstrated on such an occasion. The would-be "scientific" explanations of the camel's aptitude, ever since the writings of Pliny, have only served to add to the myth of this remarkable animal. The greatest contribution of modern times to the solution of the mystery of the camel's existence was made by the SchmidtNielsens, over 10 years ago, by studying the physiological characteristics that enable this the biggest animal living in the desert to be so perfectly adapted to its environment. To study the camel's impressive ability to tolerate desert conditions, Schmidt-Nielsen and his collaborators have wandered as far as the Sahara, the most hostile part of the camel's distributional area. With the conclusion of their investigation the puzzle of the camel has been completely solved and its physiological adaptations to the desert have become clear and rational, though still amazing. As a matter of fact, no particular trait has been identified in the camel that is not part of the general mammalian physiological pattern. In the camel only a few of these characteristics have been quantitatively changed and developed to face the hazards of life in the desert. Intense direct insolation and indirect radiation from hot atmosphere and hot soil will on a summer day tend simultaneously to increase the heat load on a camel's body. Energy created by metabolic processes will add to this 4.8 calories for each milliliter of oxygen respired by the animal at work or at rest. As for all animals exposed to a hot environment, the only way for the camel to dissipate heat when ambient temperatures approach, equal, or exceed the temperature of the body is by evaporating water. In order to counterbalance each 0.58 calorie of heat gained, 1 milliliter of water must be evaporated. The camel—an animal that cannot avoid the full impact of desert conditions because of its body size—must therefore evaporate considerable amounts of water to regulate its body temperature, and must do this in an economical and efficient way since water is so very precious in the desert. How is this accomplished? No storage of water has been detected in the camel's body, nor is its hump a reservoir of water in any sense, as many dramatic tales and superstitions want us to believe. When deprived completely of drinking water, the camel, like any other big mammal, loses weight, at a rate depending on the amount of water in the food it consumes and on the environmental conditions it is exposed to, and after a time it reaches a limit it can no longer endure. However, the camel is different from most other animals in the degree of dehydration it is able to withstand. It may lose 27 percent of its body water without damage, but at the same time it keeps the volume and water content of its blood at a relatively constant level. Then when water is available it can regain the whole loss in just a few minutes, thanks to an enormous drinking capacity. These two peculiar abilities are a clear and obvious advantage to the camel for its life in a desert area, where water sources are meager and sparsely scattered.

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Another physiological characteristic greatly reduces the use of water for thermoregulation: the temperature of the camel's large body varies greatly. Its daily fluctuation may exceed 6°C. In consequence, the slow rise of the camel's body temperature during a hot day, owing to its large mass, and the ability to tolerate a considerable rise in this temperature before starting to waste water to keep body temperature down, save a substantial amount of this precious fluid.1 Moreover, the elevated body temperature diminishes the heat differential between the body and the environment, thereby reducing the evaporation needed to prevent overheating. This mechanism of "storing" heat during the hot day and releasing it into the cool night's atmosphere removes a considerable burden from the camel, which would otherwise have to depend exclusively on the evaporative cooling mechanism. The camel's hair, which serves as an effective insulating barrier against heat flow from the environment, plays an important role in its water economy. The specialized kidney mechanism, which saves water by concentrating the urine, and the ability to excrete dry feces (Table 40) are among other characteristics adding to the camel's outstanding ability to conserve water. T a b l e 40. W a t e r c o n t e n t ( g m / 1 0 0 gm o f d r y m a t t e r ) in f e c e s of various animals. Animal Camel Camel Donkey Kangaroo rat White rat Man Cow

Feed

Water content

Hay and dates, no water Hay and dates, daily water Hay and dates, daily water Barley, no water Barley, water Mixed diet Pasture

76 109 181 83 225 200 566

Source: K. Schmidt-Nielsen, Desert animais.

(ii) The don key. Camels in a desert are generally associated in our minds with the image of a picturesque silhouette of a long caravan moving rhythmically across a vast, bare landscape following a small, long-eared donkey. This humble animal is the intimate companion of the Bedouin in his wanderings, serving him as his private conveyance, leading the camel caravans over the dusty paths, following the flocks of sheep over desert slopes, or in modern times providing the Bedouin children of the Negev with a private vehicle to school. The donkey is first mentioned in the Bible as an offering presented to Abraham by the Pharaoh of Egypt (Genesis 12:16). This is in good agreement with the modern scientific view pointing to ' A simple calculation proves the point. A rise of 6°C in body temperature of a camel weighing 500 kilograms will store about 2400 calories of heat, since the specific heat of living animal tissue is about 0.8 calorie per kilogram. Thus the camel will save 4-5 liters of water per day because this is the amount of water it would need to dissipate the 2400 calories of heat.

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North Africa as the geographic origin of the domesticated donkey. From North Africa the donkey gradually spread to southwest Asia and became a common animal in this country from the very beginning of the Early Bronze Age (excavations of Tell-Dweir and Jericho). Moreover, the ancient Jewish inhabitants of Israel were the first people to ride donkeys in addition to using them as animals of burden and work. The extremely modest food requirements of the donkey enable this useful animal to be content even with desert thistle and straw and thus to penetrate into most desolated areas of the Negev, where herds of donkeys are still to be seen near Bedouin camps. The donkey is physiologically well adapted to life in the desert, for it tolerates dehydration up to 30 percent of its body weight. In spite of this loss of water, however, its blood volume remains almost constant. Because it regulates its body temperature over a wide range of ambient conditions by evaporating sweat—at a rate three or four times that of the camel—there is significant importance in its impressive drinking capacity. In just a few minutes a donkey can guzzle a quantity of water equivalent to more than 25 percent of its body weight. (iii) The goat. This was the first ruminant to be domesticated; its remains have been found in the Neolithic layers of ancient Jericho. Where the desert surface is extremely rough and steep, where pasture is scarcest, where food and water are too meager for keeping cattle, there the goat becomes an important economic factor. Wherever there lives a Bedouin in the desert, the goat accompanies him. The black goats and the Bedouin's black tent made of goat hair attract the eye by their sheer starkness in the bare landscape of the Negev. The existence of the black-haired, blue-eyed goat—called in Arabic "maaz djebali" ( C a p r a hireus mambrica?)—and its striking contrast to the bright desert is still a mystery to us. Very little is known of its actual adaptation to the desert. We have only some indications that certain characteristics are of importance in this respect: its shiny coat is considered to have the characteristics of physical elimination of heat; like the camel, it is adept in storing heat in daytime and losing it at night. Its water economy and its kidney mechanism must be very efficient but our scientific knowledge about these matters is very scanty. (iv) The sheep. Sheep are even commoner in the Negev than goats. Their abundance in remote parts of the deserts where conditions are harsh, the food dry and sparse, and water resources few and far between is proof of their physiological adaptability to desert conditions. The local breed, the fat-tailed Awassi sheep, is popular throughout the Near Eastern deserts. It is probably an offshoot of the steppe sheep (Ovis vignei) originating in the deserts and semideserts bordering Israel. Its picture was found on an old Assyrian monument describing the booty captured at a Jewish town of southern Israel at the time of Tiglath-Pileser III or IV (8th century B.C.).

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Herodotus (c. 484-425 B.C.) describes fat-tailed sheep in Arabia. The Awassi sheep, whose name is supposed to be that of a Bedouin tribe, the Awass, living in the Euphrates region, is found in the hottest and driest of climates, having the capability of drinking but once a day and then covering a grazing area of up to 15-20 kilometers from the water source. Unlike cattle, which are forced to stand still while grazing, the sheep moves as it grazes. The lumpy tail of this breed constitutes an adaptation to the seasonal rhythm of the desert climate. The winter and early spring months (a season known as "rabia" or "pasture" by the Bedouin shepherds, for obvious reasons) is the time of the year when the desert animal has the chance of building up its food reserves for the meager summer months and so evening out nature's unbalanced seasons. The male Awassi sheep stores up to 10 kilograms of fat in its tail, the female up to 5 kilograms. By concentrating these reserves in the form of fat in one particular area, in this case the tail, instead of distributing it evenly beneath the skin, the animal is able to dissipate heat from within all over the body. Animals of the Arctic regions can serve as a counter example: the fat accumulated during the summer is deposited evenly in the deeper skin layers, thus insulating the body against the cold surroundings and conserving its heat. From information on other breeds of sheep, especially the Merino in Australia, we know that the sheep regulates its body temperature in desert conditions by evaporating water. This is done through the sweat glands of the skin and by panting, a process known to most people from dogs. During panting the ventilation of the respiratory tracts is accelerated and large amounts of water are given off from their wet surfaces into the atmosphere. These surfaces are well supplied with water from their numerous vascular blood vessels. The ability to tolerate dehydration and relatively great changes in blood volume are striking characteristics of the sheep. Its impressive drinking capacity enables it to replenish, within seconds, the whole 7-9 liters of water that it may have lost in 5 days. The fleece of the sheep has been proved to be an efficient protection against penetration of heat. When sheared, the Awassi sheep's resistance to desert heat is greatly reduced. The adeptness of the Awassi sheep in utilizing the natural food resources of extremely arid areas seems to exceed that of any other breed of sheep. The fact that under modern husbandry its milk yield has been raised from 100 liters per year per sheep, the maximum the Bedouins can obtain, to as much as 800-1000 liters points to the importance of this sheep in the agricultural development of desert areas and deserves further investigation into its physiological background. (v) The gazelle and the ibex. The livestock of the Bedouins are not the only ruminants to be found in the desert. A herd of graceful gazelles (Fig. 196) in a wide wadi bed, or a group of longhorned and black-bearded ibexes (Fig. 197) on the steep wall of a deep canyon, is an exciting sight.

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Fig. 196. Dorcas gazelle. (Courtesy of Professor Heinrich Mendelson.)

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