Table Of Content282 Annals of the
Missouri Botanical Garden
. 1 884b. Note on the laticiferous tissue of He- Webster, G. L. 1975. Conspectus of a new
classifi-
204-
vea spruceana. Quart. J. Microsp. Sci. 24: cation of the Euphorbiaceae. Taxon 24: 593-601.
206. 1987a. The saga of the spurges: A review
. of
On
. 1886. the occurrence of articulated lati- classification and relationships in the Euphorbiales.
ciferous vessels in Hevea. Linn. Soc. (Bot.) 21: Bot. Linn. Soc. 94: 3-46.
J. J.
566-573.
1987b. Evolution and
distributional history of
&
Spix, J. B. C. F. P. Martius. 1828. Pp. 612, 726 the Euphorbiaceae. Abstracts, XIV International Bo
in Reise in Brasilien. M. Lindauer, Miinchen. tanical Congress, Berlin (West) Germany.
RELATIONSHIPS OF
THE
M. 2
G. Gilbert
EUPHORBIEAE
THE
(EUPHORBIACEAE)
1
Abstract
The Euphorbieae and Hippomaneae, though both usually placed in subfamily Euphorbioideae, differ in many
inflorescence details and can be linked unambiguously only by one cryptic character: the rod-shaped starch grains in
the latex. While the Hippomaneae have inflorescences very similar to those of many other members of the Euphor-
members
iceae, the Euphorbieae have an inflorescence so specialized that one seems to be forced to relate to other
it
01 the family through a hypothetical ancestor with a synflorescence of axillary bisexual cymes more primitive than
most extant taxa possibly other than Jatropha.
A primary aim of symposium review between the Old World and New World species of
this to
is
How Euphorbia and
critically Webster's (1994) classification of the Eu- Euphorbia*? do the subgenera
phorbiaceae. This paper is an attempt to share a Lacanthis (sensu Gilbert, 1987) relate to the rest
my
speculation arising from misgivings over the sup- of the genus? Such an analysis, in view, could
posed homogeneity of the subfamily Euphorbioi- do much to clarify these relationships and thus the
demand
deae. This is not a presentation of the results of taxonomy of the tribe as a whole. It would
prolonged and detailed research but rather spec- a much greater knowledge of the possible origins
group
ulations arising while producing a routine Flora of the Euphorbieae than is available. In a
account needed.
of the Euphorbiaceae for the Flora of so morphologically isolated, speculation is
Ethiopia Hippomaneae
(31 genera, 209 species), coupled with The Euphorbieae and are includ-
a long-standing interest in Euphorbia (the largest ed within the subfamily Euphorbioideae along with
genus Pachystro-
within (Stomatocalyceae,
the Ethiopian particularly the three other tribes
flora),
succulent species. A Flora writer should delve into mateae, and Hureae) that have usually been as-
the larger scale taxonomy of those families that sociated with the Hippomaneae (Webster, 1994),
must
be covered, but rarely allowed the time to primarily on the basis of their caustic milky latex
is
carry glandular
out anything more than from nonarticulate laticifers, frequently
superficial investi-
gations on reduced flowers that always
taxa not and often highly
actually included in the Flora, bracts,
always
the following ideas must not be regarded as lack petals. This juxtapositioning has not
anything more Mueller Argoviensis (1866) and
than simple-minded speculations. been the case:
groups opposite
Ltetermining the relationships of a group as spe- Bentham (1878) placed these at
major
c,ahzed There are indeed
as sequences.
the Euphorbieae used be of ends in their
to little
c°ncern morphology between
to a Flora writer. The matter became a differences in inflorescence
conmJer
"tie more forced to
relevant two groups such that felt
with the advent of cladistics, the I
^e were the product
* the methodology demands working hy- the possibility that the similar.!.*-
a
pothesis One unusual cryptic character,
of probable groups and character of convergence.
sister
found
P^anzation. rod-shaped starch grain
Sooner or later such methods should very characteristic,
svnapo-
applied good contender for a
to the Euphorbiaceae general, and in the latex, is a
in
do have com-
thev a
*° tne Euphorbieae where morphy, which suggest i that
y particular,
in
,
re are Consistencies mon This in turn led to an attempt to re-
current generic delim- origin.
in
type
'°n. How, for instance, would analysis construct a possible ancestral inflorescence
a cladistic
ae have evolved
modern could
(Jiamaesyce, from which the plants
' very widely recognized as a
c
genus, to the various sections within Eu- most parsimoniously.
Ma have not l>een
f SUh§ ASaloma and the rest of EuP hor- The rod-shaped starch grains
h,X
'
Euphorbia. <ae,
^ • here are many other interesting problems reported in other members of the
_
.«~o never to have been
a,t,r, i.i '»..>.*>ur
S to be What i_
tackled: the relationship
is
^The
Research Cooper.*...
author was employed by the Ethiopian Flora Project, funded by the Swedish Agency for
Jevel„
„ng Countrie. (SAREC), at the time this paper was prepared.
(
""'a Department of Botany. NN,a,.,u.rr..l|
»f p add™- correspond.-,,,,-:
Ch,,,,, roject> Missour fca^fc,, arden for
Mi T 'i ( ; ;
Museum, SW7
Cromwell Road, London SBD, U.K.
199
283 288. 4.
Card. 81:
Ann. Missouri Bot.
284 Annals of the
Missouri Botanical Garden
surveyed (Rudall, 1987), and their discovery else- lanthus but also various red-flowered Euphorbia
where in the family would be a serious challenge species, pollinated by birds. In most members
of
to the taxonomic integrity of the Euphorbioideae. the Hippomaneae the styles are undivided,
long
The
toxicity of the latex has also been mentioned and tapered, and are usually characteristically
cir-
as a linking character but the major compounds cinately coiled when young. There are not many
— —
involved diterpene esters occur also in subfam- observations of pollination. The pendent
inflores-
ily Crotonoideae (Beutler et al., 1989). The pollen cences and long stigmas of some species suggest
of the Euphorbioideae is rather uniform (Punt, that wind pollination is a possibility, but other gen-
1987), but the pollen type apparently plesiomor- era have well-developed nectaries within the
is inflo-
phic; thus the similarity should be treated with rescences indicating some form of animal pollina-
caution. Morphological evidence is even less clear- tion, perhaps most often by small unspecialized
There
cut. are superficial similarities in that most insects (Bawa et al., 1985), but in at least one
taxa in both groups have a sparse to nonexistent case, Mabea occidentalis Benth. (Steiner, 1983),
indumentum of simple hairs but there are many predominantly by bats. Thus the significance of the
exceptions in both major tribes, such as species of striking differences in the styles is not clear. An-
Chamaesyce and Agaloma within Euphorbia and other possibly significant difference the frequen-
is
members of the Mabeinae and many species of cy of succulence within the Euphorbieae where
it
Stillingia within the Hippomaneae, and such ev- has clearly evolved several times independently,
idence can only be regarded as essentially negative: whereas succulence appears to be almost absent in
it does not disprove the possibility of a relationship. the Hippomaneae, recorded only from a few Bra-
The
tendency toward very reduced flowers, rare zilian species of Stillingia (Rogers, 1951).
in the family as a whole, has also been invoked to The contrast inflorescence organization be-
in
common
support a grouping. It is possible, theo- tween the Hippomaneae and the Euphorbieae seems
retically, to select a reduction series for the flowers so great that one must consider whether the sim-
Hippomaneae
within the from genera such as Ma- between them could be the result of con-
ilarities
bea, which have common
well-defined perianths and male vergence rather than an indication of
many
flowers with stamens, through to Dalember- ancestry. If the most reasonable (parsimonious)
tia, in which the male flower is reduced to a single hypothetical common ancestor has to have char-
sepal and a single stamen and the female flower acters such that would have to be placed within
it
has only remnants Crotonoi-
vestigial of the perianth. This one of the other subfamilies, notably the
sequence could be regarded as continued by the deae, rather than the Euphorbioideae, the Eu-
Euphorbieae, where the male flower is always re- phorbioideae would have to be regarded as a grade
duced
to a single naked anther and
the female rather than a clade.
flower to a naked ovary. There no case for ques-
evidence of a There seems be or
is to little
female perianth many genera Euphorbieae
in within the Eu- tioning the homogeneity of the tribe
phorbieae, including some species of Euphorbia, as clearly defined by the very peculiar inflo-
it is
other
but the only clear indication of a male rescence—the cyathium— from all
perianth, distinct
beyond an
articulation between pedicel and inflorescence types seen within the family-
fila-
ment, one
is the vestigial male perianth seen in An- naeus and other very early authors, plus
thostema and Dichostemma. Euphor >i-
There
has been a the two giants of nineteenth-century
temptation that th<
to suggest that sequence thought
this gives a aceae taxonomy, Baillon (1874),
true gu—ide to relationships, but this must be ques- cyathium was a hermaphroditic flower. How*l " •
"*
^"2
tioned could the Hippomaneae have was an >r
really given the alternative theory that
it
rise directly to the Euphorbieae? was mentioned by Lamarck as early as 1 <
The major disagree-
difference between the two groups now unquestioned, though there is still
is is
*
organic
the inflorescence
structure, which is discussed at ment in the exact interpretation of its
length below. receptacle
Details of floral morphology, most The cyathium consists of a cupular _^
notably the very alternating
different
styles, also suggest that marginal lobes usually regularly
the Euphorbieae and Hippomaneae may structure,
complex
not be glands, sometimes quite in
inser
closely related. In the Euphorbieae male flowers
the styles are closing a whorl of groups of ^
brac '
relatively short, usually divided, and have more associated ,
or below each lobe, plus their ^
aW H
j
less capitate stigmas. Studies indicate that most and female flower, often r
a single, central
varia
species are pollinated by a variety of often unspe- to a naked ovary. There quite a lot of '^
is
»Kj ^
cialized insects, the exception being a group of within theme with regard to features
this
New am
World
taxa, most obviously the genus Pedi- the number of parts within the involucre
Number 2
Volume 81 Gilbert 285
,
1994 Relationships of the Euphorbieae
amount of fusion between them and the occasional regard to the relative positions of male and female
presence of a small perianth on the male and female flowers, and must be regarded as a special case.
flowers, but no genera can be regarded as having To convert a typical Hippomaneae inflorescence
inflorescences truly intermediate between a cy- into a cyathium one must postulate a considerable
athium and any other inflorescence recorded within condensation of the main inflorescence a
axis, rel-
much common
the family. There has been debate on the atively straightforward and evolutionary
nature of the cyathium but the weight of evidence process. However, at the same time one must also
(e.g., Schoute, 1937) seems to support the scheme postulate a complete reversal in the relative position
suggested by Eichler (1878), in which each invo- of the male and female flowers or the loss of the
lucral lobe/bract subtends a monochasium of male proximal female flowers plus the de novo produc-
The
flowers. tion of a terminal female flower. latter process
The cyathium contrasts very strongly in orga- seems particularly difficult to account for unless
nization with the inflorescences of the vast majority one invokes the terminal allomorphie flowers seen
of other members of the family, including the other in some species of Acalypha. There would also
tribes placed within subfamily Euphorbioideae by have be a reversal of the general trend of the
to
An
Webster. There male
a fundamental division within reduction of the distal inflorescences. al-
is
the Euphorbiaceae between the uniovulate tribes, ternative scheme would be to derive the cyathium
with only one ovule per ovary locule, and the from a group of thyrses. Such a scenario is very
biovulate tribes, with two ovules per locule. The similar to that proposed below and must be given
biovulate tribes are distinct in so many features of consideration. The one fact against it is the cymose
anatomy and morphology that they not be arrangement of the groups of male flowers within
will
considered in detail. It might, however, be worth the cyathium. It is difficult to imagine a racemelike
making such grouping.
the observation that the axillary fascicles inflorescence giving rise to a
of flowers A more parsimonious scenario to postulate
characteristic of the vast majority of is
biovulate taxa must be considered rather special- that both the Hippomaneae and the Euphorbieae
ized reduced inflorescences. Most other uniovulate evolved from a common ancestor which had a
!nbes, including the Hippomaneae, have thyrse—a synflorescence in which an indefinite
inflores-
cences that are generally regarded as cymose, but fertile axis produced a spiral series of axillary bi-
many
show an cymes The cymes could be either
essentially racemelike organization sexual (Fig. 1).
wmcn
ln the cymose nature of the ultimate ele- dichasial or monochasial or, perhaps quite likely,
ments monochasial ultimate
is only betrayed by the fact that some of initially dichasial with
the male flowers are in very reduced cymules rather branches such as is frequently seen with Jatropha.
man
solitary as in a true raceme. The contrast The Hippomaneae inflorescence could (and surely
m
W| the Euphorbieae evolve by a simple process of reduction with
further increased by the did)
is
female
c that, as in the vast majority of the genera of the proximal cymes being reduced to single
j*
me
cymules
cymes reduced
Euphorbiaceae, the female flowers are proximal flowers and the distal to
male
the male flowers Such an arrangement of male flowers or eventually to single flowers.
distal.
pthin an elongated The Euphorbieae would have to be derived by a
inflorescence has a structural
°g»c: female more complex evolutionary process centered pri-
flowers produce bulky, longer-lived
mam
syn-
ru,ts squiring condensation of the
the transport of nutrients; male marily on a great
°Wers are produce a dense head of cymes,
usually smaller, short-lived, and only florescence axis to
puire
a perhaps response to the pro-
transient supply would be the central one, in
of nutrients.
It
fictionally becoming reduced to a single fe-
illogical to have to maintain an extra tected situation,
cymes
whorl of
% ot stem at the base of an inflorescence once male flower while the surrounding
subtending
male flowers had became male and their associated
finished, especially as the all
form an
X gtn w°uld mean stem would have bracts and ?stipular glands fused to in-
that the
k!
** that much
^° stronger mechanically. By having volucre.
cyathium has
rnale An scenario that the
**T flowers, that part of the stem does not alternative is
cyme primary female
to transport many evolved from a single with a
as nutrients for so long,
m
^°es such as Been
not need and male flowers is
to be strong enough support flower lateral
to rel-
\eofruil
e y heavy fruits, and can be shut down as soon Jatropha. Croizat (1938), in discussing
and expressed
* n« male flowers have dispersed their pollen. lauminea, accepted su< h a scenario
n involucres were the I,.-.
g said this, there an obvious exception to the belief that l-lobed
—is
pn-s.miabh Iron,
Jg«<- Acalypha which shows a bewilder- type for the Kuphorbirae, derived
dirh.iMiim.
arra of two levels of branching of a
y inflorescence types, particularly with th.- initial
Annals the
286 of
Garden
Missouri Botanical
t
Number
Volume 81 2 Gilbert 287
,
1994 Relationships of the Euphorbieae
An immediate difficulty is the frequency of 5-lobed are strictly terminal and show no tendency toward
involucres, which would be difficult to derive from the production of a synflorescence. Perhaps the
cyme
a regular dichasial but which could be ex- strictly terminal position of the inflorescence in
norm
pected as the if the involucre was the product such Jatropha a factor in their having retained
is
of the condensation of a Fibonacci spiral derived their clearly cymose organization while other groups
Two
from a thyrse. further bits of evidence argue with axillary cymes have evolved the thyrse (and
against a development from a single cyme. First cyathia?) now so widespread in the family. How-
is
&
the situation in Neoguillauminea, where the cen- ever, the most primitive species (Dehgan Schutz-
tral female flower appears to be subtended by four man, 1994, this issue), /. curcas L., does produce
separate involucres of male flowers, which indicates a synflorescence such as postulated here as the
is
that several inflorescences are involved. Second, common ancestral form for cyathia and for the
some species in Euphorbia sect. Esula (notably E. thyrses of most other uniovulate Euphorbiaceae.
cyparissioides Pax) have groups of male flowers This would seem to reinforce the view that Jatro-
and glands very pha approach an
similar to those of the involucre might represent the nearest to
intermingled within the involucre proper a pos- ancestral type for the family as a whole.
in
sible spiral series. Such a situation could be ex- In conclusion, it is suggested that it is not pos-
plained easily if the axis of the cyathium was a sible for the cyathium to have evolved from any
contracted synflorescence, but very much more inflorescence found within modern-day Hippoma-
is
difficult to explain if the structure was derived from neae (and closely allied tribes). One must conjecture
a single cyme. common ancestor belonging to
a rather primitive
Unmodified simple cymes are of rather rare neither group but rather to the Crotonoideae. If
occurrence within the family and among African this is indeed the case, it might be better to extend
taxa
are only found in Jatropha, a genus showing the Euphorbioideae to include the Crotonoideae,
a number
of other apparently primitive features, as suggested in effect by Mahlberg et al. (1987).
most
notably the an independent relationship of each
well-developed corolla and female Alternatively, if
"°wers with staminodes occasionally so well de- group to a very primitive member of the family be
m
veloped
(e.g., jr tropaeolifolia Pax) that the accepted, there might be a good case for placing
"owers
appear Hippomaneae and a subfamily of their
to be bisexual. Another unusual the allies in
character Eu-
of Jatropha is the diversity of laticifer own and restricting the Euphorbioideae to the
/Pes,
a feature
that has been an phorbieae.
interpreted as
^cattonof
&
prirnitiveness(Dehgan 1978;
Craig,
a
'1987). The cymes Literature Cited
of most species oijatro-
P a
are 105-
primarily dichasial, but in many species BaiLLON, H. 1874. Euphorbiacees. ///. Hist. PI. 2:
V-
spieata P
ax is a good example) the ultimate 256. Hachette, Paris.
Coville
ranches Bawa, K. H. Bullock, D. R. Perry, R. E.
are S., S.
usually long monochasia male
of flow-
& GRAYUM. 1985. Reproductive biology of
M. H.
Sug
Sests that there a natural tendency systems. Amer.
is trees Pollination
m lowland rainforest II.
with
the or
ganization of such cymes reduced 346-356.
for 72:
Bot.
J.
/eJ
«-minal elements to be monochasial, which would BENTHAM G. 1878. Notes on Euphorbiaceae. J. Linn.
185-267 201-204, 239 245).
1 ElchIer ' Soc, Bot. 17: (pp.
(1878)
S interpretation of the cy- McCloud &
G.
athiT Alvarado, T. G.
Beutler, A., A. B.
J.
989. Distribution of phorbol after bio-
M. CRACC.
& 1
1>ehgan
Craig (1978) Phytotherapy Re-
discussed the possibility Euphorbiaceae.
the
activity in
of
a
"^"""Ma-like 188-192.
plant being ancestral to the search 3:
Cr
^oonoideae. Notes on the Euphorbia* .m.-, with
1938.
seems CROIZAT, L.
It a distinct possibility that
64:
m Euphorbieae. Philipp. Sci.
0r °n a new genus of the J.
ancest°r of the Hippomaneae and the
Bu ?
L 397-412
Phorbieae
might
' also have had Jatropha-like & 1978. Types of lact,, rifer.
M. Cfak;.
Dehgan, E.
B.
thUS
t^l °pening UP the question of subfamily and crystals in Jatropha an.) their taxonotnir impli-
345-352.
,0nsnips. The cymes Amer. Bot. 65:
of most Jatropha species cation*. J.
"*°"™°~
to
racemelike
' • Diagrammatic representation of the hypothetical evolution of, on the left, the
of from.
[J ""cy.^lh.u^m
"'PPomaneae (and most other Crotonoideae and Acalyphoideae) and, on the nght, the
pK
shown
a cymes are ^
' S rnfl°«*cence of axillary bisexual cymes. For simplicity the mam ' and
are Tre like ^ primary On the there is a progressive elongation of the ax^
I rl!, 'y ««» dichasial. left
^"Y mam ax* form a dense clu er of
cCL " °f the cy">es. On the right there is a shortening of the to
™«. a surrounded by a whorl of all-male
and
central, terminal cyme becoming reduced to a single female flower
*e involm
whlle form an enclosing re.
associated and shpules fuse to
' subtending leaves
