Fig 1. - Euphorbia phosphorea growing in a rock outcrop, together bromeliads (Encholirium sp.) and cacti (Micranthocereus densiflorus).

Euphorbia phosphorea Mart

The largest growing succulent Brazilian Euphorbia species

Marlon Machado

Rua Visconde de Itaborai 948 apto. 303 Amaralina, CEP 41.900-020 Salvador, Bahia, Brazil

Email: marlon@brcactaceae.org The Brazilian Cacti Project: http://www.brcactaceae.org/

Introduction

"In addition to the xiquexique, palmatória, rabo-de-raposa, mandacaru, caroá, cabeça-de-frade, culumbi, cansação, favela, quixaba and the terrible macambira, we came across the much commented and much feared cumanã, a kind of liana plant with an arborescent aspect, looking exactly like the kind of cultivated plant with cylindrical leaves which is to be found in gardens. A few centimeters above the ground its stalk divides into many branches which grow in marvelous profusion, forming a huge crown which stays erect either by its own force or supported by plants growing around it. Its cylindrical branches, which have eight flutings and an equal number of veins which are not very salient, spreads out in masses over the ground, resembling an enormous polypus with millions of flexible and elastic antennae which not infrequently cover a wide surface, forming an inextricable and impenetrable network over the sparse and scrawny vegetation of this region. The sharp scythe which the soldiers of our engineering contingent [...] and of the police utilized to cut the vegetation difficultly cut this plant in the first strokes, which therefore offered an unexpected resistance to all efforts to dislodge it and clear the way." (Euclides da Cunha, in "Os Sertões", chapter two).

The last paragraph is an excerpt of the book "Os Sertões" ("Krieg im Sertao" in the German edition), of the great Brazilian essayist Euclides da Cunha, where the author describes the plant denominated cumanã, the name given by the indigenous people native of Brazil to the species that we known by the scientific name of Euphorbia phosphorea. In the chapter two of "Os Sertões", Euclides of Cunha describes the difficulties of the battalion in crossing an area of dense caatinga near the village of Juetê. The last paragraph recounts the encounter of the battalion with Euphorbia phosphorea in this region.

"Os Sertões" of Euclides da Cunha recounts a historical episode of 1896 and 1897. The government of the Republic of Brazil decided to suppress a religious sect of perhaps 7000 members, some of them violent and lawless, living in a remote rural area in the semiarid interior of Bahia; this messianic community has denied the legitimacy of the Brazilian Republic. The ensuing campaign lasted ten months, involved the deaths of hundreds of Brazilian army soldiers, and culminated in the extermination of the whole community. Besides describing in detail this that was the largest civil war in Brazil, Euclides da Cunha also describes in great detail the geography, climate, fauna and flora of the region, and also the man who lived there at that time - their way of life, their culture and their vision of the world.

Note: the plants commonly denominated xiquexique (Pilosocereus gounellei: Cactaceae), palmatória (Opuntia palmadora: Cactaceae), rabo-de-raposa (Harrisia adscendens: Cactaceae), mandacaru (Cereus jamacaru: Cactaceae), caroá (Neoglaziovia variegata: Bromeliaceae), cabeça-de-frade (Melocactus spp.: Cactaceae), cansação (Cnidoscolus urens: Euphorbiaceae), favela (Jatropha phyllacantha: Euphorbiaceae), quixaba (Bumelia sartorum: Sapotaceae) and macambira (Encholirium spectabile: Bromeliaceae) are spiny or irritant (cansação) species, and many of them grow as large colonies, thus forming true barriers which obstruct the passage of the man.

Description of the species

E. phosphorea was described by Martius in his "Reise in Brasilien" (2:726, 1828). Its specific name, phosphorea, originates from the supposed phosphorescence that this species produces. Euclides da Cunha mentions this phenomenon in "Os Sertões". He tells about the "blueish phosphorescence of the cumanãs" that can be observed at night. Other reports exist in the literature, with the luminescence sometimes reported to be produced by the latex that flow from recently cut branches, and at times reported to derive from the waxy epidermis of the plant. It is not known if the phosphorescent nature of E. phosphorea is intrinsic to the species or if this is a product of an external factor, although the latter seems to be the correct hypothesis. Rizzini (1989) comments on the hyphosis by Rodrigues that this luminescence can be caused by some parasitic fungi perhaps found only in certain geographical localities where the fungus occur. Further research is needed to verify the ocurrence and nature of the phosphorescence in this taxon.

E. phosphorea is widely distributed in the dry semiarid regions of central parts of the state of Bahia, being more rarely found also in the state of Paraíba. This species inhabits dry, exposed rocky hills and gravelly plains, within the vegetation type known as caatinga, a xerophytic vegetation defined as being a dry-deciduous thorny, low forest or scrub formation, composed of small trees, shrubs and subshrubs of entangled and usually spiny branches, that occur throughout the semiarid regions of the northeastern of Brazil. E. phosphorea grows in the ground, although it can also be found as a rupicolous, but as the rupicolous plants grow in the borders of rock outcrops whose surrounding caatinga is also inhabited by populations of this species, it can mean that the rupicolous habit is not an ecological preference as the plants are not restricted to the rocks, but it is the result of the establishment of some plants in suitable places of the rock outcrops, being that these plants have provenance from the surrounding areas where this species can be found in greater numbers.

Fig. 2 - Euphorbia phorphorea often forms dense colonies, here in the border of a rock outcrop in the city of Morro do Chapéu.

E. phosphorea grows as a much-branched tall shrub to a small tree, attaining a height of up to 6 meters when growing amongst denser and taller caatinga vegetation, but usually staying with a average height of 2 meters. The plants form a small trunk when growing amidst the caatinga, but they branch from the ground level when growing as a rupicolous. The branches have variable length, but once they stop growing they do not resume its growth, and new growth is obtained only by the production of more branches. Branches of Euphorbia phosphorea are straight and grow upright or a bit inclined (in this case the leaning of the branches is due to their weight, all new growth have the tendency to grow upright), and range in average from 1 to 3 cm in diameter (though the short basal trunk can reach 5 cm or more in diameter).

A particular characteristic of E. phosphorea are its polygonal branches, with a number of angles ranging from 6 to 9, the usual number being 7 or 8. The sides of these polygonal branches are plane of slightly concave, conferring a slightly canaliculate appearance to the branches.

Each branch display a number of nodes, separated by internodal spaces (the space between two consecutive nodes) of variable lenght, but usually around 5 cm. The nodes are arranged in a ascending helical pattern along the branch. The edges of these angled branches, which from now on will be denominated ribs, are intimately related to the nodes: from each node three ribs originate, and each node also receive three ribs originated from other nodes. The disposition of the ribs also follows a well-defined pattern: two of the ribs originating in a given node will end in a same posterior node, while the third rib will end in a different posterior node. This pattern is the same found in E. sipolisii and also ocasionally found in E. attastoma; these two species are related to E. phosphorea and will be discussed further on. In a specimen of E. phosphorea with 8 ribs, whose nodes are arranged in a counterclockwise ascending helix (the more common configuration), the left rib leaving a node will end in the second node that follows that node in the ascending helix; the central and right nodes leaving a node will end in the third node that follows that node in the ascending helix (see diagram 1).

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Fig. 3 - A seedling of Euphorbia phosphorea. The bromeliad is Encholirium sp.

Fig. 4 - The very new growth of E. phosphorea is colored in an intense hue of red. With the development of the new branch the reddish color fade away. It is possible to observe rudimentary leaves in the nodes at the top of the new branch. These leaves are soon deciduous. The older branches are conspicuously covered in way, what confer to them a glaucous pale green color, and at times the cover of wax is so intense that the branch appear grayish-white in color.

Fig. 5 - In these new branches it can be clearly observed the pattern in which the ribs develop in E. phosphorea. In these particular branches, the new nodes are generated along a counterclockwise ascending helix. In each node, the left rib leaving a node converge to the second node that follows that node in the ascending helix; the central and right nodes leaving a node converge to the third node that follows that node in the ascending helix (see diagram 1).

Diagram 1. The pattern in which the ribs appear in the sequence of helically ascending nodes. The numbers indicate the sequence in which the nodes originate. Note that some of the nodes appear twice in the diagram, for easiness of understanding.

The epidermis of the branches of E. phosphorea is light green in color, having a thick cuticle covered in wax, which confer to the branches a glaucous appearance. At times the cover of wax is so intense that the branches assume a grayish-white coloration (see fig. 4). In older branches, the outermost section of the cuticle tends to break and become rough and irregular, with pieces of wax falling from the surface of the branch. Another particular characteristic of Euphorbia phosphorea is that the new growth is flushed with red, often in a intense wine color (see fig. 4). The red color of the new developing branches quickly fade away as the branches develop.

Mature branches of E. phosphorea are aphyllous, but this species does bear leaves, though the leaves are rudimentary and soon caducous, appearing only in the shoot apexes of developing branches. The leaf is succulent, lanceolate with a small groove in its adaxial side. Each leaf measure about 1 mm in diameter and from 3 to 6 mm in length, and are reddish in color.

The cyathium of E. phosphorea consists of 5, more rarely 6 glandular nectaries, which surround one pistillate flower and from 0 to 3 staminate flowers; very rarely the cyathium is consisted of only staminate flowers. The cyathium have a diameter of 8 mm in average. A characteristic of this and related species is that the cyathial glands have a pair of symmetric appendixes, which are prolonged and curved inwards, resembling two small horns. The horns measure from 1 to 3 mm in length. As pointed out by Rizzini (1989), these horns are highly reminiscent of jaws of leafcutter ants (Atta sp.). The surface of all the cyathial parts is strongly verrucose. The fruit is an exserted tripartite capsule, linked to the cyathium by means of a short stalk (see fig. 9).

The cyathium of E. phosphorea is colored wine-red (see fig. 8 & 9), and this was supposed to be the only color that the cyathia of this species possess. However, the author recently found some specimens with yellowish horns (fig. 6 & 7). These specimens were found amidst a population of E. phosphorea bearing typical red cyathia, located to the west of the city of Morro do Chapéu. This finding narrows still more the distinction between this taxon and E. attastoma, a closely related species which have yellowish cyathia in some of its populations.

Each node of a branch can produce an aggregate of 1 to 10 cyathia. In the flowering season, the branches are often completely covered with flowers (see fig. 10 & 11).

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Cyathia of Euphorbia phosphorea:

Fig. 6 & 7 - Cyathia with yellowish horns in the cyathial glands, found in a few specimens of a population that have predominantly red cyathia, in Morro do Chapéu, Bahia.

Fig. 8 & 9 - Usual red cyathia of plants from the same population as above. It can be observed the verrucose surface of the cyathial glands and of the fruit and fruit stalk.

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Fig. 10 - This picture shows the crown of a flowering specimen of Euphorbia phosphorea. In the flowering season, the branches are completely covered with flowers.

Fig. 11 - Close-up of a flowering branch.

The Euphorbia phosphorea complex

There are three other Brazilian Euphorbia species which are very closely related to E. phosphorea, forming a group of species distinct and well differentiated from the other succulent Euphorbia species that occur in Brazil. The species that compose this group of related species, collectively denominated the Euphorbia phosphorea complex, are Euphorbia sipolisii N. E. Brown, Euphorbia attastoma Rizzini, and Euphorbia holochlorina Rizzini. There are two other species, Euphorbia pteroneura A. Berger from Mexico, and Euphorbia weberbaueri Mansfield from Peru, which are related to E. phosphorea and belongs to this group as well, but these species will not be examined here.

E. sipolisii (fig. 12) occur restricted to a small mountainous region in the northeast region of the state of Minas Gerais, around the city of Diamantina. This species differ from E. phosphorea in account of its much smaller habit, usually less than 100 cm in height, normally staying around 50 cm but reaching up to 150 cm in the northernmost populations. The plants branch heavily from ground level, forming thick bushes. The main characteristic of E. sipolisii that easily distinguish it from E. phosphorea are its consistently four-ribbed branches, which are quadrangular in cross-section, due to the areas between the ribs be almost flat. The cyathia of E. sipolisii are not very different from those of E. phosphorea, being distinct only in account of its slightly smaller size, and the pair of horns of the glands being shorter and V-shapped. As in E. phosphorea, the developing branches are reddish, often strongly so.

E. attastoma (fig. 13) is also found in northern Minas Gerais, and it was originally described for plants found in the mountains around the city of Grão Mogol. However, it was also collected in other parts of Minas Gerais - the variety xanthochlora was described for plants found around the cities of Pedra Azul and Medina. E. attastoma is also found in Minas Gerais in the mountains of Bocaiúva, Monte azul, and possibly throughout the mountains of the northern Espinhaço range in Minas Gerais. Recent collections from Bahia seems also to represent this taxon (Eggli, 1994), although the number of ribs in the plants from these populations is higher (7-8) than the typical number for this species (6).

If these populations found in Bahia prove to be really E. attastoma, then the occurrence of E. attastoma in Bahia demonstrate that this species have a wider distribution than it was thought at fisrt. However, these populations, whose cyathia answer the description of E. attastoma var. xanthoclora (they bear yellowish cyathial glands), can prove to more properly belong to E. phosphorea, since this species can also bear yellowish cyathial glands (see fig. 6 & 7).

E. attastoma is very closely related to E. phosphorea. It is characterized by a more shrubby growth, remaining smaller than E. phosphorea, attaining an avegage height ranging from 100 to 150 cm. E. attastoma do not develop a small trunk, branching from ground level as does E. sipolisii. E. attastoma was described as having consistently six ribs in its branches. The collections from Bahia have 7-8 ribs, which is more characteristic of E. phosphorea (this species can have from 6 to 9 ribs, the usual being 7 or 8). A further difference noted by Rizzini (1989) is that E. attastoma have more canaliculate branches, that is, the area between the ribs is somewhat concave, whereas in E. phosphorea the area between the ribs is almost flat.

For the author, the main distinguishing characteristic of E. attastoma is the fact that the three ribs that leave each node will converge all to only one node, in contrast with E. sipolisii and E. phosphorea, where, from the three ribs that leave each node, only two will converge to the same node, the other rib will unite with a third node. This arrangement is so far only known to occur in E. attastoma, and is very consistent - all the populations of this species that the author have investigated in the field, in the cities of Pedra Azul, Grão Mogol and Bocaiúva in Minas Gerais, possesses this characteristic.

E. attastoma has two varieties, that differ mainly in the color of the cyathial glands: Euphorbia attastoma var. attastoma Rizzini bear red cyathia, whereas Euphorbia attastoma var. xanthochlora Rizzini bear yellowish cyathia. The cyathia of E. attastoma is very similar to the cyathia of E. phosphorea, differing in the fact of that the tips of the horns of the cyathial glands are somewhat curved inwards, a characteristic more strongly noticed in the horns of E. attastoma var. xanthochlora. Developing branches of E. attastoma also display a reddish color.

E. holochlorina is found in only one locality, the Serra do Cristalino moutains, in the city of Nova Venécia of the state of Espírito Santo. This species is reported in the original description to be very similar to E. attastoma in all the vegetative traits, the only differences being in the greener color of the branches, and in the cyathia, which in E. holochlorina is pale green in color and have erect glands forming a narrow cup-like structure. The two horns of each gland are also erect or ascending. This species was not investigated in the field by the author, and will not be examined further on.

The species of the Euphorbia phosphorea complex appear to be very closely related, and probably form a distinctly monophyletic group. Three species in special, E. phosphorea, E. attastoma and E. sipolisii, seems to constitute a nearly contiguous cline in a north-south trend. Although each species presents its own set of particular characteristics which uniquely distinguish one species from the others, the species’ boundaries are remains nebulous, and intermediate forms are to be found.

E. sipolisii, found around Diamantina, is the smallest species of the group. However, this species displays a significant increase in average size from the southern populations to the northern populations, being that the plants found in the mountains to the north of the small village of Inhaí (a district of Diamantina located in the northern area of the city, boundaring with the city of Bocaiúva) have an average height of nearly 150 cm. In these populations we often find plants with five ribs instead of the usual number of four.

The populations of E. sipolisii from Inhaí are separated from the nearest populations of E. attastoma, found in the mountains of the district of Engenheiro Dolabela in the south of Bocaiúva, by some 60 km. Although this distance seems to be large enough, it is to be noticied that the mountains in the intervening region are not discontinuous, rather they form a uninterrupted range of mountains with plenty of suitable habitats in which both species can inhabit and are likely to occur.

The area between Inhaí and Engenheiro Dolabela lacks road access and are practically inaccessible by all means, except by slow and careful foot travel over rocky and broken terrain, thus making any exploration a slow and arduous task. Therefore this area is practically unexplored. It will be interesting to determine in the future if this region possess populations of plants with intermediate characteristics. E. attastoma from Engenheiro Dolabela is already very variable, with specimens possessing five or even four ribs at times.

E. attastoma, by its turn, is very similar to E. phosphorea. It differ mainly in the smaller and more shrubby growth and smaller number of ribs, which are arranged in a different way than in E. phosphorea. But, although E. phosphorea grows larger, reaching to the size of a small tree when growing in the ground and even developing a small single trunk, this species assume a smaller and more shrubby growth when growing on rocks, reaching only up to 200 cm and branching from near ground level, thus approaching E. attastoma in appearance. The existence in Bahia of populations of plants supposedly belonging to E. attastoma, but which have 7-8 ribs, blur still more the boundaries between the two species, narrowing the distinction between them.

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The three species of the Euphorbia phosphorea complex that seem to form a cline:

Fig. 12 - Euphorbia sipolisii, found in Diamantina, Minas Gerais. The specimen shown in the photo have about 30 cm in height. The small cactus in the picture is Uebelmannia flavispina.

Fig. 13 - Euphorbia attastoma, found in Grão Mogol, Minas Gerais. The specimen shown in the photo have about 100 cm in height.

Fig. 14 - Euphorbia phosphorea, found on rocks in Morro do Chapéu, Bahia. The specimen shown in the photo have about 200 cm in height.

Up to now I have been discussing only the vegetative and morphological features of the species of the Euphorbia phosphorea complex, and ignoring the reproductive structures of these species, their cyathia. The reason for that is that the size and shape of the cyathium is practically the same in all three species, varying only in minor details of color, size and shape of the horns found in the cyathial glands. These characters are variable within each species, and display a wide range of variability even among plants of one same population. Furthermore, the size, shape and color of the horns are also dependent of environmental factors, such as hydric stress, amount of sunlight and of nutrients in the soil, among others. Shaded plants usually develop smaller cyathia with poorly developed horns. This is usually observed in plants in cultivation. Thus, although surely each species possesses its own set of cyathial characteristics, these characteristics are so variable that possibly they don’t have taxonomic significance.

The evident clinal variation in vegetative characteristics between the three species is probably more important in devising the possible evolution of the ancestral taxon which gave rise to these species. From north to south, we can observe a progressive diminution in height and in number of ribs from E. phosphorea to E. attastoma, and from this species to E. sipolisii.

Perhaps of major significance is the change in ecological preferences along this north-south cline: while E. phosphorea is preferentially terricolous, growing in the dry soils of caatinga areas (only rarely this species is found growing as a rupicolous, but in these cases the plants usually grow in the very borders of rock outcrops surrounded by caatinga vegetation where E. phosphorea occur in much greater quantities), E. attastoma and E. sipolisii are predominantly rupicolous, growing in pockets of soil found in the rock outcrops.

The reason for this can rely on the fact that the caatinga areas are much drier than the southern regions inhabited by E. attastoma and E. sipolisii; the lack of sufficient moisture in the rocky environments restrict the growth of E. phosphorea in the rocks, obligating this species to inhabit in the soil of the caatinga, an environment that favored taller plants of E. phosphorea due to the competition with other shrub and tree species. In the areas of occurrence of E. attastoma and E. sipolisii, the more humid environment favor the growth of a denser and taller vegetation in the soil areas, with which E. attastoma and E. sipolisii cannot compete; thus, in these regions, only the rock outcrops provide suitably competition-free habitats where these species can establish themselves, and the higher humidity allow these species to grow in pockets of soil in the rocks. The lack of taller vegetation to compete with probably lead to the dwarf size of these species, when compared to E. phosphorea. E. attastoma, growing in a region intermediate between the area of occurrence of E. phosphorea and E. sipolisii, displays intermediate characteristics and a higher vegetative diversity as a result.

The process of speciation leading to the differentiation of E. phosphorea, E. attastoma and E. sipolisii is still unfinished, with areas where these species overlap in characters, but it seems that these three taxa represent already distinct entities.

References:

Cunha, Euclides da (1994). Krieg im Sertao. Suhrkamp, Fr.

Eggli, U. (1994) Xerophytic Euphorbias from Brazil. The Euphorbia Journal 9:11-21, illus.

Machado, marlon (1998). The caatinga vegetation of northeastern Brazil. Cact. Succ. J. (US) 70(6):304-310.

Rizzini, C.T. (1989) Cactiform Species of Euphorbia from Brazil (Euphorbiaceae). Rev. Brasil. Biol. 49 (4): 979-997, 14 figs.

Additional pictures

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