"New" data relating to the evolution and phylogeny
of some carnivorous plant families
Keywords: evolution physiology taxonomy.
In recent times several papers appeared dealing with the systematic arrangement
of several families of carnivorous plants by DNA sequence alignment and
homology comparison (Albert et al., 1992; Conran & Dowd, 1993;
Cameron et al., 1995). One rather surprising result of this work
was an apparent affinity of Byblidaceae to several families of "sympetalous"
dicotyledons. This could mean that Byblis is related to the order
Scrophulariales which also contains the carnivorous family Lentibulariaceae
and the sub-carnivorous genus Ibicella (Martynia p.p., Martyniaceae/Pedaliaceae
Another even more striking result is the grouping of Droseraceae, Drosophyllaceae
(the separation of Drosophyllum from Droseraceae is also supported
by DNA analysis), Dioncophyllaceae, Ancistrocladaceae, Nepenthaceae, Plumbaginaceae,
Polygonaceae, and Simmondsiaceae together in one clade to which the couple
Tamaricaceae/Frankeniaceae is the closest sister clade (see Figure 1).
This grouping is so striking because it unites families which have been
assigned to numerous orders in previous systems (e.g. Saxifragales, Theales,
Aristolochiales, Primulales, Caryophyllales, Euphorbiales), formerly believed
to constitute widely distinct groups. But it is especially interesting
because it now brings several carnivorous families into close proximity
to each other. Additionally, a phytochemical characteristic, viz. the
presence of the acetogenic naphthoquinone plumbagin in Droseraceae, Drosophyllaceae,
Dioncophyllaceae, Ancistrocladaceae, Nepenthaceae, and Plumbaginaceae,
and biosynthetically related anthraquinones in Polygonaceae (Hegnauer,
1989) lends further strong support to the assumption that this grouping
is not an artificial one (plumbagin is only found in very few other families
of flowering plants like Ebenaceaewhich group close to Ericales according
to DNA data and thus do not seem to belong to the "carnivorous" plumbagin
cladeand several monocotyledonswhich are certainly not closely related
to this group). The genetical methods cannot yet resolve the exact relationships
within the new clade defined (cf. the unresolved trichotomies in the diagram,
this will certainly improve as soon as additional data become available),
and character distributions within this clade are somewhat reticulate.
Instantly, the question arose if morphological characteristics could
be found in the new cousins of the carnivores which indicated a sub-carnivorous
condition in these (i.e. predispositions to the carnivorous habits presumably
evolved later on). An examination of Ancistrocladaceae (consisting only
of the small palaeotropical genus Ancistrocladus which is known
for some time to be the closest relative of Dioncophyllaceae, sharing
e.g. similar pollen and petiole structure and the unique naphthyl-isoquinoline
alkaloids, cf. Bringmann & Pokorny, 1995) yielded no compelling results.
But even the closest relatives of Triphyophyllum (viz. the other
two members of Dioncophyllaceae, Habropetalum and Dioncophyllum,
which are non-carnivorous) do not show any obvious sign of the striking
features observable in the trapping leaves of Triphyophyllum.
Nevertheless, there are some apparently bridging features to Nepenthaceae
(which overlap in some parts of the distributional range with Ancistrocladaceae),
viz. a rather unusual anatomy of the petiole base (Metcalfe, 1951).
The more striking it is when we direct our attention to another, superficially
rather inconspicuous family, viz. Plumbaginaceae. This family is characterized
by the possession of specialized glands secreting lime and/or mucilage
(licopolian or mettenian glands). These glands were studied in some detail
more than hundred years ago (Wilson, 1890). Already then a close resemblance
of these to the salt glands found in Frankeniaceae and Tamaricaceae was
noted. The recent genetical studies mentioned showed that phylogenetic
relations between these families seem likely. Additionally, glands resembling
to some degree the sessile ones of Plumbaginaceae can be observed on the
leaf surfaces of Ancistrocladus and Nepenthes.
More recent research (Rachmilevitz & Joel, 1976; Fahn, 1979) revealed
anatomical details of the specialized mucilage calyx glands of Plumbago.
These glands show some peculiar features which are found to recur in the
tentacles of Drosera, Drosophyllum and Triphyophyllum.
They are borne on multicellular stalks with an epidermis and several layers
of underlying parenchyma, thus constituting emergences. The glandular
portion consisting of several layers of secretory cells is separated from
the parenchyma of the supporting stalk by a single or few layers of cutinized
cells forming an endodermis exactly like in the tentacles of the mentioned
carnivores. Additionallyand this is almost unique in this groupa vascular
strand sometimes enters the parenchymatous core of the stalk for some
distance. Therefore, the calyx glands of Plumbago display features which
render them "almost complete" precursors or evolutionary prototypes of
the tentacles of the mentioned adhesive carnivorous plants. Some species
of Plumbago (e.g. P. tristis) and many representatives of
Ceratostigma and Dyerophytum have either glabrous calyces
or emergences on the calyx which do not bear a glandular head. Plumbagella,
a seemingly more advanced (annual, temperate) descendant of Plumbago
(perennial, subtropical to tropical) does share the glandular emergences
with this genus. It has been argued that the bristles and sticky secretions
of the calyx of these genera (which together form the subfamily Plumbaginoideaethe
other subfamily, viz. Staticoideae apparently lacks plumbagin) aid in
seed dispersal by animals, ensuring an attachment to the coat or plumage
of these (Fahn & Werker, 1972). The single-seeded fruits of these
plants remain in the calyx and are easily detached together with it from
the fruiting pedicels. Subsequent observations (Rivadavia, 1996) on P.
auriculata showed that small ants were found trapped on the sticky
glands of the calyx of this species. Thus, it can be assumed that an additional
function in at least the glandular species is the exclusion of crawling
insects from the flowers, thereby favouring flying pollinators which more
effectively assure cross pollination (crawlers tend to visit all the flowers
of the inflorescence of a single individual while flying insects more
frequently change between several different inflorescences and individuals).
The following hypothetical course of events can be formulated:
1. An evolution of the floral biology affecting first seed dispersal
(from glabrous to bristly calyx) led to the formation of bristly emergences
on the outer (abaxial) sepal epidermis. Recent representatives of the
"primitive" stage are found in Dyerophytum, the more "advanced"
condition is frequent in Ceratostigma and few species of Plumbago.
2. A further evolution of floral biology now affecting pollination (from
bristly calyx to glandular calyx) led to glandular emergences, the vascularization
of which could have rendered the process of secretion more effective.
The glandular portion of these emergences was probably derived from the
sessile glands of the leaf surfaces (suggested by structural similarities
between both). Recent representatives of the "advanced" condition being
many species of Plumbago and the single species of Plumbagella.
3. The crawlers frequently caught by the glandular emergences (which
later became tentacles) were in some way utilized for the nutritional
purposes of the plantsthe adhesive trap was thus formed. Once this trapping
strategy was successful, the other carnivorous features (like the irritability
of the glands and the secretion of digestive enzymes) could have appeared
by chance and were conserved by selection because they rendered ad hoc
advantages over the individuals which did not display them.
4. The translocation of the tentacles to foliar surfaces (N.B. Plumbago
europaea has vascularized bristles and Plumbagella micrantha
has even stalked glands on the leaf margins, Drosophyllum has the
tentacles on the abaxial surface of the leaves corresponding to the situation
in the Plumbago calyx) rendered the traps more efficient in Drosophyllum
5. The integration of perceptive, motile, and digestive functions in
the tentacles as well as a translocation to the upper, adaxial surface
of the leaves constituted further refinements of the traps in Droseraceae
6. At some stage of this development, the springtrap mechanisms of Aldrovanda
and Dionaea diverged from possibly adhesive precursors (but
not necessarily from Drosera).
Fortunately, recent examples of these stages are extant (many of which
found in the single subfamily Plumbaginoideae). Of course it must be borne
in mind that the respective representatives are descendants of evolutionary
intermediates and not the intermediates themselves.
Now it may be asked how Nepenthaceae could be integrated into the "emergent"
scenery. But there may even be an answer to this one presented by Plumbaginaceae.
Wilson (1890:244) writes, discussing Aegialitis annulata: "The
petiole is of considerable length, and amplexicaul to a great degree.
The inspection of a piece of epidermis from its base at once reminds one
of the 'digestive surface' of Nepenthes", and when he continues
"The similarity is only superficial, for in Nepenthes the glands
lie at the termination of vascular traces, whereas the mucilage-glands
of Aegialitis and all other Plumbagineae have no such connection,"
he thereby possibly even emphasizes this similarity because the same degree
of parallelism can be observed between Plumbago/Plumbagella (where
the glands are sometimes approached but in most cases not reached by vascular
traces) and the adhesive carnivorous plants (in which the glands lie at
the termination of the vessels). About Plumbago scandens,
Wilson (1890:247) writes: "Spiral vessels pass up a greater or less distance
into the stalks. Seeing, however that vessels are found penetrating simple
emergences e.g. in Ceratostigma, etc., no special significance
attaches to them in connection with the glands" but in the light of the
notes made above, it seems that very special significance attaches to
them in connection with carnivorous plant evolution!
It might be added that Aegialitis is considered a relict in the
mangroves of the tropics of southeast Asia and north Australia, not closely
related to any of the remaining members of Plumbaginaceae (which are predominantly
more temperate). The glands on the surface of the leaves probably serve
the purpose of secreting the excess of salt taken up with the brackish
water the plants grow in. The similarity to Nepenthes is certainly
not very far reaching and the pitchers of this genus remain unique organs
in the plant kingdom.
It is interesting to see that most of the data mentioned here were known
and published more than hundred years ago and only fifteen years after
carnivory in plants was appreciated scientifically (Darwin, 1875). Nevertheless,
only genetic and phytochemical results forced our awareness towards the
conspicuous morphological parallels between Plumbaginaceae and several
I wish to thank the Director and staff at the Botanical Garden of Würzburg
who supplied flowering material of Plumbago indica. Special thanks
are due to Mr. Fernando Rivadavia from Sao Paulo, Brazil, who made important
field observations on Plumbago auriculata mentioned above, and
who sent liquid preserved material of this species.
Albert, V. A., Williams, S. E. & Chase, M. W. (1992) Carnivorous
plants: phylogeny and structural evolution, Science 257(5076):1491-1495.
Bringmann, G. & Pokorny, F. (1995) The Naphthylisoquinoline Alkaloids,
Cameron, K. M., Chase, M. W. & Swensen, S. M. (1995) Molecular
evidence for the relationships of Triphyophyllum and Ancistrocladus,
Conran, J. G. & Dowd, J. M. (1993) The phylogenetic relationships
of Byblis and Roridula inferred from partial 18s ribosomal
RNA sequences, Pl.Syst.Evol. 188:73-86.
Darwin, C. (1875) The Insectivorous Plants, London.
Fahn, A. (1979) Secretory Tissues in Plants, Academic Press.
Fahn, A. & Werker, E. (1972) Anatomical mechanisms of seed dispersal.
in: Kozlowski, T. T. (ed.), Seed Biology, Academic Press.
Hegnauer, R. (1989) Chemotaxonomie der Pflanzen, vol.8, Birkhäuser.
Metcalfe, C.R. (1951) The Anatomical Structure of the Dioncophyllaceae
in Relation to the Taxonomic Affinities of the Family, Kew Bull.:351-368.
Rachmilevitz, T. & Joel, D. M. (1976) Ultrastructure of the Calyx
Glands of Plumbago capensis Thunb. in Relation to the Process of Secretion,
Rivadavia, F. (1996) personal communication.
Wilson, J. (1890) The Mucilage and other Glands of the Plumbagineae,
Ann. Bot. 4:231-258.