espinhos e variegacao

8/11/2019 Espinhos e Variegacao

1/7

Journal of Theoretical Biology 224 (2003) 483489

Why do some thorny plants resemble green zebras?

Simcha Lev-Yadun*

Department of Biology, Faculty of Science and Science Education, University of Haifa, Oranim, Tivon 36006, Israel

Received 28 April 2002; received in revised form 1 May 2003; accepted 7 May 2003

Abstract

The rosette and cauline leaves of the highly thorny winter annual plant species of the Asteraceae in Israel ( Silybum marianum)

resemble green zebras. The widths of typical variegation bands were measured and found to be highly correlated with leaf length,

length of the longest spines at leaf margins and the number of spines along leaf circumference. Thus, there is a significant correlationbetween the spinyness and strength of variegation. I propose that this is a special case of aposematic (warning) coloration.

r 2003 Elsevier Ltd. All rights reserved.

Keywords: Aposematic coloration; Herbivory; Silybum marianum; Thorns; Zebra

1. Introduction

Aposematic coloration in animals is well known.

Until recently (Lev-Yadun, 2001), aposematic colora-

tion in plants has received only marginal, scant

attention, and only a handful of studies have discussedit (Hinton, 1973;Harper, 1977;Wiens, 1978;Rothschild,

1980; Williamson, 1982; Knight and Siegfried, 1983;

Smith, 1986; Lee et al., 1987; Givnish, 1990; Archetti,

2000). Several of these authors (Knight and Siegfried,

1983; Smith, 1986; Lee et al., 1987; Archetti, 2000)

rejected the idea that this phenomenon could occur in

plants. Hinton (1973) briefly proposed that the bright

colors of flowers are aposematic. Because flowers of

some species are known to be poisonous to animals, the

poisonous species are probably aposematic, whereas the

others perform Batesian mimicry (Hinton, 1973).

Flowers, however, are usually colored as advertisements

for pollinators, and it is difficult to distinguish between

two cooccurring functions of the same coloration.

Harper (1977)in his seminal essay proposed in a single

sentence that the association of unpalatability with

visual signals might have selected much of the large

variation in leaf form, variegation, and other characters.

Harper (1977)also indicated that what we know about

warning coloration comes from predatorprey inter-

actions in which the prey are animals and that botanists

have been reluctant to accept adaptations that are

commonplace for zoologists.Wiens (1978)briefly raised

the question of whether the variegated or mottled

patterns of coloration that characterize plants, particu-

larly leaves, are aposematic, and gave several examplesof poisonous plant parts with bright colors. Moreover,

Wiens (1978) proposed that unprotected plants might

mimic the variegated patterns. Rothschild (1980) pro-

posed that in certain poisonous plant species carote-

noids might serve in aposematic coloration.Williamson

(1982) proposed that brightly colored (red or red and

black) seeds lacking an arillate or fleshy reward (e.g.

Erythrina, Ormosiaand Abrus) might be aposematically

colored to warn seed eaters of their toxicity.Knight and

Siegfried (1983) raised the question of whether green

fruit signals unpalatability and proposed that green does

not provide enough contrast to be aposematic. Smith

(1986) hypothesized that leaf variegation may be

aposematic but concluded that, for the vine species

(Byttneria aculeata) he studied, the variegation was

related to herbivory, mimicking leaf mining damage.

AlthoughSmith (1986) rejected the aposematic hypoth-

esis, he gave a clear and detailed formulation of the

aposematic hypothesis for plants: The benefits to

the plant of chemical defense against herbivores would

be greater if herbivores avoided such plants altogether,

rather than testing leaves for palatability, and so causing

some damage. A distinct leaf color pattern linked

with chemical defense might function in this way.

ARTICLE IN PRESS

*Corresponding author. Tel.: +972-4-983-8827; fax: +972-4-983-

2167.

E-mail address: [email protected] (S. Lev-Yadun).

0022-5193/03/$ - see front matter r 2003 Elsevier Ltd. All rights reserved.

doi:10.1016/S0022-5193(03)00196-6


2/7

Polymorphism for leaf color should then coincide with

polymorphisms for chemical defense. M.ullerian and

Batesian mimicry could result in evolution of similar

patterns of variegation, with or without associated

toxicity, among other species which have herbivore

species in common with the model species (Smith,

1986, p. 284).Givnish (1990)noted thatSmiths (1986)rejected hypothesis regarding the aposematic value of

leaf variegation should also be considered. Lee et al.

(1987)concluded that anthocyanins in developing leaves

of mango and cacao are not aposematic. Olfactory

aposematism in poisonous plants was also proposed

(Eisner and Grant, 1981; Launchbaugh and Provenza,

1993).

White variegation is known in many plant species. It

was proposed that variegation has several functions that

can compensate for the reduced photosynthetic ability

of white tissues (Allen and Knill, 1991).Morgan (1971)

showed that variegated leaves appeared in Hydro-

phyllum appendiculatum under open spring canopy,

whereas under closed canopy, when light is low, solid-

colored leaves are formed. Cahn and Harper (1976a)

showed that the frequency of variegated leaves in

Trifolium repens decreased with increasing grass length

and concluded that this was related to grazing. More-

over, in a field experiment with rumen fistulated sheep

that enabled sampling of what was grazed, they found

that unmarked leaves were clearly preferred over

marked ones (Cahn and Harper, 1976b). Smith (1977)

gave evidence that albino seedlings of Phyllostachys

bambusoides can confer a competitive advantage to

green siblings over inter-specific competitors. Niemelet al. (1984) showed that in variegated leaves of Acer

pseudoplatanus insect herbivores had favored white

areas over mixed and green areas. This preference

correlated well with the chemical properties of white

areas that contained more nutrients and less phenolics.

Smith (1986)showed that in B. aculeata the variegated

morph is more common in open habitats. Givnish

(1990), who has published the most comprehensive

study on the possible benefits of leaf mottling, proposed

that camouflage from color-blind vertebrate herbivores

was the major selective agent for variegated leaves in

short forest herbs that grow as understory in the flora of

the north-eastern USA

Recently,Lev-Yadun (2001)showed that two types of

conspicuousness of thorns are typical of many plant

species originating from several continents and belong-

ing to various families: (1) colorful thorns and (2) white

spots and stripes associated with thorns in leaves and

stems. Both phenomena predominate the spine system

of the spiniest taxonthe Cactaceae in which about

90% of the species have white markings associated with

the colorful thorns. Similarly, most spines in Agave are

colored and in about 25% of the species there are stripes

along the margins that mark the spines. Dozens ofAloe

species also have colorful thorns and many Aloespecies

have both colorful thorns and white markings. In the

genus Euphorbia, colorful thorns and white or whitish

variegation or white markings associated with thorns

also predominate. It was also proposed that multi-

colored spines have a specific value as they provide more

possibilities that some will be visible to herbivores thatare color blind to a certain sector of the spectrum. A

white signal has a distinct advantage over a colorful one:

color-blind animals can see it, and it is more visible to all

under low illumination. Thus, vegetal aposematic

coloration that communicates between plants and

herbivores about being thorny has been proposed

(Lev-Yadun, 2001).

Here, I show that a very thorny annual rosette species

of the Asteraceae in Israel have white markings that

resemble a zebra. Such a unique and conspicuous

appearance should have a function, which I tried to

determine. The significant correlation between the

conspicuousness of the white variegation and spinyness

enabled the proposition that this is a special case of

vegetal aposematic (warning) coloration that commu-

nicates between plants and herbivores about being

spiny.

2. Materials and methods

Silybum marianum (L.) Gaertner (=Carduus maria-

nus) is a medicinal plant widely used in traditional

European medicine. The information concerning this

plant has recently been reviewed (Morazzoni andBombardelli, 1995) and summarized as follows. The

plant grows in the Mediterranean region, Central

Europe, Central and East Asia, North and South

America and Southern Australia. It is a typical ruderal

plant. Many of the plants form a large rosette in the

early winter, and later, slender stems 20250 cm high

grow from the apex of the rosette. All parts of the plant

are very thorny and the inflorescences have a crown of

thick, strong, ca. 46 cm long and very sharp thorns. Its

name comes from the conspicuous zebra-like appear-

ance of its leaves. According to an old legend, the white

marks on its leaves were formed when Mary nursed

baby Jesus while sitting under this plant and some of her

milk dripped on the leaves and since then the plant has

been variegated. The genus name Silybum derives from

the ancient Greek word sillybon (a pendant) that was

used by Dioscorides almost 2000 years ago. The species

S. marianum is also known as Holy thistle, Marys

thistle or milk thistle (Morazzoni and Bombardelli,

1995). In Israel, the plant grows all over the humid

Mediterranean district and parts of the Negev desert

(Feinbrun-Dothan, 1978) and is eaten by Arab villagers.

The inner parts of young stems and young leaves are

used as green salad. Roots, young leaves and stems are

ARTICLE IN PRESS

S. Lev-Yadun / Journal of Theoretical Biology 224 (2003) 483489484


3/7

eaten cooked after they have been immersed in water for

several hours, the young inflorescence is cooked like

artichoke and eaten, tea substitution is made of dry

leaves and roasted seeds are also eaten (Dafni, 1984).

However, its uses as a food plant are limited, and its

major importance is its uses as a medicinal plant. A

purified extract of the fruits (silymarin) and its majorconstituent (silybin) are used to treat liver diseases

(Morazzoni and Bombardelli, 1995).

The typical width of the white stripes, the length of

zebra-like rosette leaves, the total number of marginal

thorns in a leaf and the length of the largest thorns were

measured in the most common zebra-like plant S.

marianum (L.) Gaertner. Many fully developed cotyle-

dons and 100 fully developed rosette leaves ranging in

length from 2.8 cm (the first rosette leaves in young

rosettes) to 92 cm, each one from a different rosette,

were collected from plants of all sizes from young

seedlings to rosettes that were more than a meter in

diameter. In each leaf, its length, the width of a typical

variegation band and the length of the longest spine

were measured and the total number of spines along its

margins was counted. The continuity of the majority of

variegation was also determined. For statistical analysis

a non-parametric Spearmans correlation (StatMost for

Windows) was used.

3. Results

In the field, the white, large and zebra-like marking

on the upper surface of the rosette leaves (Fig. 1) isconspicuous from several up to dozens of meters

according to leaf size and number of rosettes in a group.

In S. marianum, a very common zebra-like plant, the

ontogeny of the leaves shows a clear positive correlation

between the number and length of thorns along the

margins and the extent of white variegation. The

well-developed green cotyledons have no spines and no

variegation (Fig. 2). The young rosette leaves are flat

and form a two-dimensional thorn system (Figs. 2 and3). When the rosettes grow, the leaves become wavy,

forming a three-dimensional spine system, with a much

more developed variegation (Fig. 4). The wavy large

leaves are much better protected because there are spines

that capture a space, in contrast to the flat spine layer of

the small rosettes. In small, 2.84.0 cm long, rosette

leaves, the white stripes are ca. 1 mm wide and a

considerable proportion of the zebra-like variegation is

not continuous (Fig. 3). There is considerable variability

in the thickness of the white stripes (Figs. 4 and 5), but

in most large, mature plants the white stripes are wider

ARTICLE IN PRESS

Fig. 1. A typical rosette ofS. marianum at mid season, two months

before flowering about 60 cm in diameter, ca. half of its final size. The

white network of stripes on the upper surface gives it a zebra-like

appearance. The larger rosette leaves are not flat and form a three-

dimensional thorn system. Such appearance characterizes three highly

thorny annual rosette species of the Asteraceae common in Israel:

Silybum marianum, N. syriaca and Seolymus maculatus.

Fig. 2. Well-developed green cotyledons that have no spines and no

variegation. The first pair of young rosette leaves, with their typical

thin and non-continuous variegation are also seen. They are flat and

form a two-dimensional thorn system.

Fig. 3. In the first whorls of rosette leaves, when the plants are small,

the white stripes are usually only about 1 mm wide and a considerable

proportion of the variegation is not continuous.

S. Lev-Yadun / Journal of Theoretical Biology 224 (2003) 483489 485


4/7

than 4mm (Fig. 5). In the small rosette leaves, the

longest marginal spines are not longer than 1 mm and

their number per leaf ranges between ca. 25 and 40

(Table 1). These values gradually increase and in the

large rosette leaves of mature plants their length ranges

between ca. 70 and 92 cm, the white stripes are usually

about 56 mm (range 37 mm) wide, and the zebra-like

variegation is continuous (Table 1). The marginal spines

in rosette leaves of all sizes are of various lengths. The

shorter ones are about 1 mm long, whereas the longestmarginal spines are 37 mm long and their length

correlates with the width of the white stripes (Table 1).

The total number of marginal spines in a large leaf

ranges between ca. 1060 and 2225. Although the white

markings are wider when plants are larger, the size of

the leaves increases more than the size of the white

stripes. Still, large variegated rosettes are conspicuous

from a distance of over 10m and are much more

conspicuous than small ones.

There was a strong correlation between rosette leaf

lengths and the widths of the stripes of white variegation

(r 0:81; n 100 p50:001), rosette leaf lengths and

maximal lengths of the spines along the margins

(r 0:83; n 100 p50:001) and rosette leaf lengths

and the number of spines along the margins (r 0:97;

n 100 p50:001). Similarly, the signal (widths of the

stripes of white variegation) and the maximal lengths of

the spines along the margins (r 0:80; n 100

p50:001) and the number of spines along the margins

(r 0:81;n 100p50:001) were also highly correlated.

4. Discussion

Here, I show that thorny leaves in a rosette plantspecies of the Asteraceae are conspicuous because they

have zebra-like white markings. The regular appearance

of white variegation on the rosette leaves of this species

and two other common rosette species of the Asteraceae

(Notobasis syriaca (L.) Cass. and Scolymus maculatus

L.) indicates that such morphology should have an

advantage.

The white marking should have some cost in

resources, in addition to the burden of being conspic-

uous to herbivores. The large white areas on the leaves

should reduce their photosynthetic potential. As the

plants are winter annuals, reducing heat load or excess

solar radiation does not seem to be the selective

advantage for this phenomenon. We must therefore

look for another explanation for this phenomenon.

The fact that in the field, the zebra-like marking of the

annual rosettes is conspicuous from several up to dozens

of meters according to leaf size and number of rosettes

in a group seems on first view to opposeGivnishs (1990)

conclusion that white leaf mottling serves as camouflage.

Givnish (1990), however, studied understory species that

grow in a habitat characterized by a mixture of dark and

light spots, and here, I studied a species of open, well-

illuminated areas, thus there is no contradiction.

ARTICLE IN PRESS

Fig. 4. Wavy, lobed leaves, forming a three-dimensional thorn system

develop when the rosettes continue to grow. The white variegation is

gradually becoming more conspicuous and continuous. Length of leaf

part in figure is 16 cm.

Fig. 5. The typical, several millimeter wide white stripes in a large

rosette leaf of a large plant. Length of leaf part in figure is 16 cm.



5/7

I propose that concerning this issue, white mottling

may act as camouflage in undergrowth in the forest as

proposed by Givnish (1990) and as conspicuous apo-

sematic coloration in open, well-illuminated areas.

Recently, it has been proposed (Lev-Yadun, 2001)

that aposematic (warning) coloration is common in four

thorny taxa (cacti,Agave,AloeandEuphorbia) that have

colorful thorns and white or other marking that

highlights them. I propose that such white markings

have a specific value. When a certain herbivore is color

blind to a certain sector of the spectrum, is color blind

altogether, or when illumination is not strong, white

marking increases the possibility that the aposematic

signal will still be visible. There are good indications that

although many mammalian herbivores have only

ARTICLE IN PRESS

Table 1

Thorns and variegation in the rosette leaves ofS. marianum(each leaf

originated from a different plant

Leaf

number

Length

(mm)

Width (mm) of

typical

variegation line

Length of

largest spines

(mm)

Total number of

spines in leaf

margins

1 28 1* 1 322 28 1* 1 33

3 32 1* 1 37

4 32 1* 1 42

5 37 1* 1 30

6 37 1* 2 34

7 41 1* 2 26

8 42 1* 1 24

9 42 1* 1 42

10 43 1* 2 32

11 43 1* 1 41

12 46 1* 2 33

13 46 1* 1 36

14 47 1* 2 51

15 48 1* 2 36

16 50 1* 2 4617 51 1* 2 35

18 54 1* 2 45

19 62 1* 1 93

20 67 1* 3 59

21 68 2* 2 48

22 70 1* 1 51

23 70 2* 2 65

24 71 1* 1 43

25 74 1* 2 84

26 75 1* 2 40

27 76 2* 2 70

28 84 1* 2 86

29 86 2* 2 80

30 88 2* 2 129

31 90 1* 2 7532 92 2 2 74

33 100 1* 2 90

34 102 1* 2 111

35 103 1* 2 87

36 107 1* 2 111

37 111 1* 3 95

38 115 1* 3 94

39 117 2* 2 117

40 144 3* 2 131

41 152 2* 3 127

42 183 3* 3 149

43 192 3 3 262

44 196 3 3 170

45 200 3 3 146

46 210 2 3 22547 210 4 3 286

48 223 4 3 226

49 230 2* 4 491

50 265 4 4 580

51 266 3 4 310

52 287 5 4 406

53 300 5 3 624

54 317 6 4 557

55 345 3 3 600

56 350 4 2 927

57 360 5 3 574

58 360 3 3 580

59 367 3 3 764

60 370 3 3 840

Table 1 (continued)

Leaf

number

Length

(mm)

Width (mm) of

typical

variegation line

Length of

largest spines

(mm)

Total number of

spines in leaf

margins

61 380 5 3 461

62 391 3* 3 549

63 396 3 3 67264 398 5 3 646

65 403 5 3 715

66 410 3 3 778

67 420 3 3 705

68 434 3* 3 565

69 436 4 3 592

70 446 3 3 526

71 455 3 4 720

72 460 3 3 946

73 480 3 3 770

74 485 2* 2 610

75 510 6 4 869

76 522 3* 4 935

77 523 4 3 704

78 535 4 3 111179 547 4 3 985

80 560 2* 3 855

81 564 3 3 783

82 570 5 5 1051

83 574 2 3 1333

84 604 4 3 886

85 610 5 4 775

86 620 3 3 1175

87 625 2 3 862

88 657 4 3 870

89 660 4 4 926

90 673 3 4 1360

91 675 6 4 1360

92 690 4 3 937

93 710 5 5 144594 755 5 3 1062

95 760 5 4 1685

96 815 5 5 1300

97 853 6 4 1218

98 865 3 4 1890

99 885 7 7 2140

100 920 4 4 2225

*Non-continuous line.



6/7

dichromatic vision, which is a much weaker color vision

ability than human color vision, they can see colors to a

certain extent (Jacobs, 1993;Kelber et al., 2003). In the

last several millennia, the vegetation of the Near East

suffered a continuous impact of grazing. Under such

conditions, thorny plants, which were grazed less than

non-thorny ones became very common (Zohary, 1962,1983). Sheep, goats and cattle are the major grazers,

while horses, donkeys and camels were of secondary

importance (Sasson, 1998). In the past, before the

spread of agriculture and massive human-related im-

pact, wild grazers, such as gazelles, deer, goats, rabbits

and cattle, were probably the common grazers.

The question of honest signaling is important for the

evaluation of the evolutionary consequences of the

conspicuous spines, but determining honesty in biologi-

cal signaling is difficult. The honesty is maintained by

the herbivores that taste the plants. The strong

association of the size of white marking with the size

and number of thorns in the species examined makes it

clear that this plant species is so thorny that it can afford

its consciousness, i.e. the strong signal is honest. My

painful field experience clearly showed me the honesty of

the signal. Every time I sampled large wavy leaves for

measurements I was wounded. Only an insect or a snail

that can move between the spines (or a very hungry large

herbivore) would eat them, but when and where they

grow there are enough non-spiny plants to graze on.

When the rosette leaves dry up in the summer and the

markings are not seen any more, some of the dry

rosettes are eaten by the herds. I propose that grazers

learn to identify these plants. As the season progresses,they become larger, spinier, more conspicuous and

probably suffer less damage if at all. Since most of the

poisonous materials in the plants accumulate in the

seeds, at the end of the life cycle, there seems to be no

chemical aposematism in this case.

When in a certain habitat there is an increase in the

proportion of conspicuous thorny plants, because they

are associated with white marking, for a period long

enough for an evolutionary change, M .ullerian mimicry

may lead to the establishment of defense guilds (see

Waldbauer, 1988). Because there are three zebra-like

plant species in the East Mediterranean region, I

propose that such a defense guild evolved in these

winter annual thorny rosette plants of the Asteraceae

that have white markings that give them the appearance

of green zebras.

The last issue that I wish to discuss is the possibility

that the variegation evolved as a protective mechanism

against insect herbivores. There are two related relevant

hypotheses concerning this issue. The first hypothesis is

that the variegation serves as mimicry of tunnels of flies

belonging to the Agromyzidae. The larvae of flies of

this group eat the photosynthetic tissues in the leaves,

which results in white variegation resembling that of

S. marianum. Thus, the variegation might serve as

mimicry of an already infected leaf to deter female

Agromyzidae flies from laying eggs. The second, related

hypothesis is that such stripes reduce insect landing on

the leaves in general, as was proposed for the evolution

of zebra stripes as defense against tsetse flies (Waage,

1981;Brady and Shereni, 1988;Doku and Brady, 1989;Gibson, 1992). Although the significant correlations of

variegation with thorn number and length presented

here seem to be the major explanation for the evolution

of variegation, some role of protection against insects of

the white variegation should not be ruled out. If the

insect protection hypothesis is also true, the evolution-

ary advantage of zebra-resembling leaf variegation was

two-fold and selected for by both vertebrate and

invertebrate herbivores.

Acknowledgements

I thank Gidi Neeman, Gadi Katzir, Moshe Inbar,

John R.G. Turner and an anonymous reviewer for their

helpful comments on the manuscript.

References

Allen, J.A., Knill, R., 1991. Do grazers leave mottled leaves in the

shade? Trends Ecol. Evol. 6, 109110.

Archetti, M., 2000. The origin of autumn colours by coevolution.J. Theor. Biol. 205, 625630, doi:10.1006/jtbi.2000.2089.

Brady, J., Shereni, W., 1988. Landing responses of the tsetse fly

Glossina morsitans morsitans Westwood and the stable fly

Stomoxys calcitrans (L.) (Diptera: Glossinidae and Muscidae) to

black-and-white patterns: a laboratory study. Bull. Entomol. Res.

78, 301311.

Cahn, M.G., Harper, J.L., 1976a. The biology of the leaf mark

polymorphism inTrifolium repens L. 1. Distribution of phenotypes

at a local scale. Heredity 37, 309325.

Cahn, M.G., Harper, J.L., 1976b. The biology of the leaf mark

polymorphism in Trifolium repens L. 2. Evidence for the selection

of leaf marks by rumen fistulated sheep. Heredity 37, 327333.

Dafni, A., 1984. Edible Plants in Israel. Association for Nature

Protection, Tel Aviv (in Hebrew).

Doku, C., Brady, J., 1989. Landing site preferences of Glossinamorsitans morsitans Westwood (Diptera: Glossinidae) in the

laboratory: avoidance of horizontal features? Bull. Entomol. Res.

79, 521528.

Eisner, T., Grant, R.P., 1981. Toxicity, odor aversion, and olfactory

aposematism. Science 213, 476.

Feinbrun-Dothan, N., 1978. Flora Palaestina, Vol. III. The Israel

Academy of Sciences and Humanities, Jerusalem.

Gibson, G., 1992. Do tsetse flies see zebras? A field study of the visual

response of tsetse to striped targets. Physiol. Entomol. 17, 141147.

Givnish, T.J., 1990. Leaf mottling: relation to growth form and leaf

phenology and possible role as camouflage. Funct. Ecol. 4,

463474.

Harper, J.L., 1977. Population Biology of Plants. Academic Press,

London.

ARTICLE IN PRESS



7/7

Hinton, H.E., 1973. Natural deception. In: Gregory, R.L., Gombrich,

E.H. (Eds.), Illusion in Nature and Art. Duckworth, London,

pp. 97159.

Jacobs, G.H., 1993. The distribution and nature of colour vision

among the mammals. Biol. Rev. 68, 413471.

Kelber, A., Vorobyev, M., Osorio, D., 2003. Animal colour

visionbehavioural tests and physiological concepts. Biol. Rev.

78, 81118.Knight, R.S., Siegfried, W.R., 1983. Inter-relationships between type,

size and color of fruits and dispersal in Southern African trees.

Oecologia 56, 405412.

Launchbaugh, K.L., Provenza, F.D., 1993. Can plants practice

mimicry to avoid grazing by mammalian herbivores? Oikos 66,

501504.

Lee, D.W., Brammeler, S., Smith, A.P., 1987. The selective advantages

of anthocyanins in developing leaves of mango and cacao.

Biotropica 19, 4049.

Lev-Yadun, S., 2001. Aposematic (warning) coloration associated with

thorns in higher plants. J. Theor. Biol. 210, 385388, doi:10.1006/

jtbi.2001.2315.

Morazzoni, P., Bombardelli, E., 1995. Silybum marianum (Carduus

marianus). Fitoterapia 66, 342.

Morgan, M.D., 1971. Life history and energy relationships ofHydrophyllum appendiculatum. Ecol. Monogr. 41, 329349.

Niemel.a, P., Tuomi, J., Siren, S., 1984. Selective herbivory on mosaic

leaves of variegatedAcer pseudoplatanus. Experientia 40, 14331434.

Rothschild, M., 1980. Remarks on carotenoids in the evolution

of signals. In: Gilbert, L.E., Raven P, H. (Eds.), Coevolution

of Animals and Plants. University of Texas Press, Austin,

pp. 2051.

Sasson, A., 1998. The pastoral component in the economy of hill

country sites in the intermediate bronze and iron ages: archaeo-

ethnographic case studies. Tel Aviv 25, 351.

Smith, A.P., 1977. Albinism in relation to competition in bambooPhyllostachys bambusoides. Nature 266, 527529.

Smith, A.P., 1986. Ecology of leaf color polymorphism in a tropical

forest species: habitat segregation and herbivory. Oecologia 69,

283287.

Waage, J.K., 1981. How the zebra got its stripesbiting flies as

selective agents in the evolution of zebra coloration. J. Entomol.

Soc. S. Afr. 44, 351358.

Waldbauer, G.P., 1988. Aposematism and Batesian mimicry. Measur-

ing mimetic advantage in natural habitats. Evol. Biol. 22, 227259.

Wiens, D., 1978. Mimicry in plants. Evol. Biol. 11, 365403.

Williamson, G.B., 1982. Plant mimicry: evolutionary constraints. Biol.

J. Linn. Soc. 18, 4958.

Zohary, M., 1962. Plant life of Palestine (Israel and Jordan). The

Ronald Press Company, New York.

Zohary, M., 1983. Man and vegetation in the Middle East.In: Holzner, W., Werger, M.J.A., Ikusima, I. (Eds.), Mans

Impact on Vegetation. Dr W. Junk Publishers, The Hague,

pp. 287295.

ARTICLE IN PRESS


espinhos e variegacao

Documents