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Botanical Journal of the Linnean Society, 2009, 161, 329–356. With 12 figures
Murderous plants: Victorian Gothic, Darwin and
modern insights into vegetable carnivory
Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3DS, UK
Department of Botany, Natural History Museum, Cromwell Road, London SW7 5BD, UK
Scientific Associate, Department of Botany, Natural History Museum, Cromwell Road, London SW7
Received 20 October 2009; accepted for publication 3 November 2009
Darwin’s interest in carnivorous plants was in keeping with the Victorian fascination with Gothic horrors, and his
experiments on them were many and varied, ranging from what appears to be idle curiosity (e.g. what will happen
if I place a human hair on a Drosera leaf?) to detailed investigations of mechanisms. Mechanisms for capture and
digestion of prey vary greatly among the six (or more) lineages of flowering plants that have well-developed
carnivory, and some are much more active than others. Passive carnivory is common in some groups, and one,
Roridula (Roridulaceae) from southern Africa, is so passively carnivorous that it requires the presence of an insect
intermediate to derive any benefit from prey trapped on its leaves. Other groups not generally considered to be
carnivores, such as Stylidium (Stylidiaceae), some species of Potentilla (Rosaceae), Proboscidea (Martyniaceae) and
Geranium (Geraniaceae), that have been demonstrated to both produce digestive enzymes on their epidermal
surfaces and be capable of absorbing the products, are putatively just as ‘carnivorous’ as Roridula. There is no clear
way to discriminate between cases of passive and active carnivory and between non-carnivorous and carnivorous
plants – all intermediates exist. Here, we document the various angiosperm clades in which carnivory has evolved
and the degree to which these plants have become ‘complete carnivores’. We also discuss the problems with
definition of the terms used to describe carnivorous plants. © 2009 The Linnean Society of London, Botanical
Journal of the Linnean Society, 2009, 161, 329–356.
ADDITIONAL KEYWORDS: carnivorous plants – insectivorous plants – phylogenetics – proto-carnivory.
Carnivorous or insectivorous plants have long
induced fascination in men, and they are among the
most popular plants in cultivation; they are often
offered for sale in garden centres and over the Internet. There are many amateur botanical societies that
focus upon them. The first living specimen of Dionaea
muscipula Ellis ex L. came to the attention of the
populace of London in 1768, an event that ‘caused a
sensation throughout Europe’ (Magee, 2007: 49).
Indeed, Linnaeus is reported to have declared
*Corresponding author. E-mail: [email protected]
‘miraculum naturae’ (Magee, 2007) upon seeing D.
muscipula. Prior to this event, John Bartram had
sent Patrick Collinson, a London botanical collector,
several plant parts, after the specimen sent by Governor Dobbs of North Carolina had failed to arrive
(Magee, 2007). Bartram used a popular name for D.
muscipula, tipitiwitchet, a somewhat ribald Elizabethan term for vulva (McKinley postscript to Nelson,
1990). This connection between female sexuality
and carnivorous plants continued into 19th century
England and may have had something to do with
their popularity and continued public fascination.
Insectivorous plants epitomize Victorian England’s
cultural interest in the Gothic form in literature,
architecture and art and, in terms of natural history,
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
bizarre spectacles. These ‘queer flowers’, as Grant
Allen described insectivorous plants in 1884, reached
a zenith of popular and artistic attention during the
mid to late 19th century. Allen’s essay demonstrated
the lure of the insectivorous plant as a floral femme
fatale and in richly descriptive language described
its ‘murderous propensities’ (Allen in Smith, 2003).
Smith (2003) considered Swinburne’s poem ‘The
Sundew’ in relation to Allen’s essay and Darwin’s
(1875) study on insectivorous plants. He noted that
‘both Swinburne’s poem and Darwin’s book were
prominent elements in a cultural fascination with the
sundew that extended from the 1860s well into the
1880s’, and ‘in the aftermath of Insectivorous Plants
the potentially subversive moral and cultural implications of “The Sundew” become more difficult to
ignore’ (Smith, 2003: 130–131).
In one of the most fanciful of Victorian stories, the
German explorer Carl Liche and members of the
cave-dwelling Mkodo tribe were described as making
a trip through the Madagascan jungle. At one point,
they come upon an amazing sight: a large plant with
a bulbous trunk resembling a 2.5-m pineapple with
eight elongate leaves, 3–4 m long, studded with hooklike thorns surrounding a depression filled with
honey-sweet liquid. At the top of the tree are a set of
long, hairy green tendrils and tentacles, ‘constantly
and vigorously in motion, with . . . a subtle, sinuous,
silent throbbing against the air.’ The story goes on to
say that one of their women is forced at javelin point
to climb the trunk. Then ‘the atrocious cannibal tree,
that had been so inert and dead, came to sudden
savage life. The slender delicate palpi, with the fury
of starved serpents, quivered a moment over her
head, then as if instinct with demoniac intelligence
fastened upon her in sudden coils round and round
her neck and arms; then while her awful screams and
yet more awful laughter rose wildly to be instantly
strangled down again into a gurgling moan, the tendrils one after another, like great green serpents, with
brutal energy and infernal rapidity, rose, retracted
themselves, and wrapped her about in fold after fold,
ever tightening with cruel swiftness and savage
tenacity of anacondas fastening upon their prey.’ ‘The
great leaves slowly rose and stiffly, like the arms of a
derrick, erected themselves in the air, approached one
another and closed about the dead and hampered
victim with the silent force of a hydraulic press and
the ruthless purpose of a thumbscrew.’ [‘Liche, 1881’
(almost certainly a fictitious author; see below) cited
by Osborn (1924)].
Some readers took this account seriously. Travellers
had been returning from the jungles of the world
with astonishing stories: ferocious man-like apes,
vine-shrouded lost cities. Gorillas and the Mayan
ruins turned out to be real. Why not the man-eating
tree in far away Madagascar, when at home in
England there was a vegetable carnivore, the sundew,
known to everyone? In Victorian times, Gothic stories
combining horror and romance prevailed, and the
story of a man-eating tree or any carnivorous plant
was utterly exciting. Vegetable man-eaters matched
the characters used in the supernatural tales about
ghosts, haunted mansions, werewolves etc.
Combined with the fantastic findings in natural
history by travellers, these man-eating trees tickled
the fancy of writers. Buel (1887), for example, in his
book Sea and Land included a section on carnivorous
plants, in which, following a description of the action
of Dionaea Ellis and Drosera L., he then wrote about
a plant from Central Africa (possibly Liche’s Madagascan plant) and tropical America, where it is known
as Ya-te-veo [I-see-you.] (Fig. 1), ‘that is not contented
with the myriad of large insects which it catches and
consumes, but its voracity extends to making even
humans its prey’. What fate awaited the ‘unfortunate
traveller’? ‘The body is crushed until every drop of
blood is squeezed out of it and becomes absorbed by
the gore-loving plant, when the dry carcass is thrown
out and the horrid trap set again.’ Due to the spines
Figure 1. The man-eating tree Ya-te-veo reported to occur
in Central America by Buel (1887).
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
reported to pierce the body of the victim, Buel made
an analogy to the maiden, a torture instrument ‘of
the dark ages’ (with inward pointing spikes) which
‘was made, somewhat crudely, to represent a woman,
hence the name applied to it’. Following more gory
details about ulcers resulting from puncture wounds
inflicted by the plant and mention of the ‘hundreds of
responsible travelers [who] declare they have frequently seen it’, he concluded this section as follows:
‘All of which, however, I am inclined to doubt; not that
there is no foundation for such statements as travelers sometimes make about this astonishing growth,
but that the facts are greatly exaggerated’. Thus even
writers aiming to provide a vivid, but true, account of
the wonders of nature managed to confuse real and
fictional carnivorous plants.
Liche’s story was adopted by Chase Osborn (1924)
in his book Madagascar, Land of the Man-Eating Tree.
Osborn said missionaries had vouched for the existence of the tree. No one has ever laid eyes again on
this carnivorous horror, or on the Mkodo tribe for that
matter, and Ley (1955) wrote that the Madagascan
man-eating tree, the Mkodo tribe and even Carl Liche
himself were all fabrications. It is nevertheless a
gruesomely good story that may have its origins in
older works, such as the True History of Lucianus
Samosatensis, written in the 2nd century AD, in which
female grapevines consumed sailors who tried to mate
with them (note again the references to carnivorous
plants being alluring and female).
Darwin himself was fascinated by carnivorous
plants. He came to believe, after much experimentation, that the movement-sensing organ in sundews
(Drosera) is far more sensitive than any nerve in the
human body (Darwin, 1875). American naturalist
Mary Treat, who studied many of these plants in her
garden and understood their functioning in detail,
discovered the function of bladderwort (Utricularia
L.) traps (Fig. 2). She communicated regularly with
Darwin about carnivorous plants and helped him
understand their habits better (Sanders & Gianquitto, 2009). Another female correspondent and
Figure 2. Utricularia minor L., cultivated at RBG Kew. Photograph taken by Maarten J. M. Christenhusz.
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
friend, Lady Ellen Lubbock (the wife of Darwin’s
great supporter Sir John Lubbock, later Lord
Avebury) wrote a poem on reading Darwin’s Insectivorous Plants and sent it to him (see Milner, 2009). It
included the verse:
I never trusted Drosera
Since I went there with a friend,
And saw its horrid tentacles
Beginning all to bend.
We are accustomed to think of plants as being
immobile and harmless, and there is something deeply
unnerving about the thought of carnivorous plants.
The ongoing fascination with these stories, exaggerating the traits of real-life carnivorous plants, indicates
the deep horror we feel towards the idea of being
devoured by a plant. No wonder the myths of the
man-eating tree have stayed with us for centuries.
In 20th century Anglo-American culture, we saw a
shift from the Gothic form to kitsch with the show
Little Shop of Horrors and the character Audrey II –
an extraterrestrial carnivorous plant that constantly
cries ‘feed me’ (Fig. 3). The Life of Pi (Martel, 2001)
featured a floating mat of carnivorous algae. Vegetable carnivores have also been adopted in science
fiction stories such as Parasite Planet (Weinbaum,
1935), in which a plant on Venus eats humans. In The
Fellowship of the Ring (Tolkien, 1954), hobbits fall
asleep and find themselves eaten by a plant. Huge
carnivorous trees are also dangers of the forests in
Beyond the Deepwoods (Steward & Riddell, 1998).
In Comet in Moominland (Jansson, 1973) Moomintroll saves the Snork Maiden from the twining arms
of a poisonous bush of the ‘dangerous Angostura
family’ with his penknife.
A carnivorous plant, Tentacula, is also featured in
the Harry Potter series (Rowling, 1998), building upon
the romantic but horrific idea of plants devouring
Figure 3. The man-eating plant Audrey II from the film
Little Shop of Horrors (Film Group Inc.; Griffith, 1960).
people. Even some Pokémon characters (e.g. Bellsprout, Weepinbell and Victreebell; Pokémon, 2009) are
based on carnivorous plants, bringing them into
popular modern culture. More recently, the discovery
of Nepenthes attenboroughii A.S.Robinson, S.McPherson & V.B.Henrich (Robinson et al., 2009) has stimulated a flurry of internet-dispersed rumours of
‘rat-eating plants’ (e.g. Instructables, 2009) and
so a fascination with the ‘murderous propensities’
of carnivorous plants continues to capture the public
Turning to a more serious side of the subject, several
definitions of botanical carnivory have been proposed,
but most researchers still consider at least some
species lacking some aspects to nonetheless be fully
carnivorous. The basic definition includes at least the
ability to absorb the products of decomposition, either
directly on the leaves or through roots in the soil,
thereby increasing their fitness, ultimately leading to
increased seed production. Including absorption by
roots of nutrients released through one method of
decay or another means that nearly all plants are
capable of a degree of carnivory, and indeed this
minimal definition is the one we follow in this paper (at
least in terms of the taxa we treat). However, researchers who follow the ‘six lineages of carnivore’ argument
(see below; Ellison & Gotelli, 2009) would add as well
the provisos that these plants should also exhibit some
means of (1) attracting prey to their traps (glistening
glandular hairs being a minimal common attractant),
(2) capture of prey and (3) their digestion. Digestion in
many species generally held to be carnivores is not
necessarily through enzymes secreted by the plant
itself, but this can be achieved via enzymes secreted by
bacteria, fungi or even the stomachs of other animals
that eat trapped prey with the subsequent absorption
of nutrients released by deposition of their faeces on
nearby soil. The minimal glandular apparatus that
secretes mucilage or other compounds needed to trap
animals is widespread in angiosperms, almost to the
point of being universal, at least in eudicots. Croizat
(1961) thought that carnivory was an ancestral
angiosperm attribute, a concept not far removed from
the sentiment of the previous sentence; extant fully
developed carnivores are merely more refined cases of
underlying capacities present in all flowering plants.
Formation of tanks into which prey and vegetable
detritus fall and decay is also frequent, particularly in
the commelinid monocots (e.g. bromeliads and others;
see below). Proving that there is a net energetic benefit
to carnivory when its occurrence is frequent and subtle
makes it more difficult (what would one use as the
background case for angiosperms?). Studies have
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
shown that construction costs and scaling relationships for leaf traits in ‘true’ carnivores are substantially greater when traps are active (Ellison & Gotelli,
2009), but relatively few taxa have developed such
complex traps; active traps occur in only two families,
Droseraceae and Lentibulariaceae. In the great majority of the taxa we discuss below, carnivory is simpler,
and in terms of leaf construction the costs are less and
scaling relationships much like those of ‘normal’
plants. Overall, angiosperms of many types may be
involved in a degree of carnivory and be ‘protocarnivorous’; perhaps we should be more curious about
why more plant species have not developed a ‘taste’ for
animal-derived nutrients.
Phylogenetic studies of DNA sequences have greatly
aided efforts to assemble a complete tree of life for all
angiosperms; based on this understanding of flowering
plant phylogeny, full-blown carnivory has evolved in
the angiosperms at least six times (Albert, Williams &
Chase, 1992; Chase et al., 1993). These phylogenetic
studies have also provided insights into morphological
evolution of the varied mechanisms employed by
plants to attract, retain, kill and digest animals and
finally absorb the released nutrients. Darwin (1875)
himself was certain that there had been several independent origins of carnivory, and this assumption has
been broadly accepted by plant taxonomists since the
time of Darwin. However, acceptance of polyphyly of
carnivorous plants has been against a backdrop of
major disputes over which groups of carnivores were
closely vs. distantly related and to which other groups
of angiosperms they are related (e.g. Hutchinson,
1973; Cronquist, 1981; Thorne, 1992; Takhtajan,
1997). Suggestions of relationships between groups of
plants that we now know to be spurious were put
forward by some of the most prominent botanists of
their time: Hooker (1874; based on an idea from
Linnaeus), for example, believed that species of Sarracenia L. were not only related to but had also evolved
from waterlilies as a result of the move onto dry land.
Takhtajan (1969) placed Sarraceniales near the
ranalean complex, which included Nymphaeales,
Papaverales and Ranunculales. It is equally clear that
the origins of carnivory have been clouded by both
convergent and divergent evolution and, before the
advent of molecular phylogenetics, this subject was at
an impasse and could no longer progress.
The first phylogenetic assessment of carnivore relationships was that of Albert et al. (1992), and this
paper set the stage for more complete subsequent
investigations by other authors. Albert et al. (1992)
were particularly interested in the degree to which the
carnivorous syndrome could provide evidence about
general macroevolutionary patterns and process in
flowering plants. Indeed, this must have also been the
reason why Darwin studied these plants and wrote
Insectivorous Plants (Darwin, 1875). Extreme specializations were thought to provide important insights
into more general phenomena, such as the functions of
sticky glands. Sticky, mucilage secreting, glandular
hairs occur commonly throughout the angiosperms,
and their exact functions are not always easily determined. Many angiosperms are undoubtedly passive
carnivores; once an insect has been trapped by sticky
glands, even if prevention of herbivory is the actual
role of these hairs, its subsequent decay can provide
nutrients, taken up by roots of the trapping plants.
This sort of passive carnivory is clearly taking place in
the southern African Roridula Burm. ex L. (Roridulaceae, Ericales), aided by the action of a Nemo-like†
bug that is unharmed by its host and lives its entire life
on these plants, depositing on the soil around the
plants its faeces, to the benefit of its host.
The ability to produce water-storage structures,
whether through epiascidiation (inrolling of the
abaxial leaf lamina with subsequent fusion of the
margins as in Nepenthes L. and Sarracenia) or tank
formation (as in the bromeliads Brocchinia Schult.f.
and Catopsis Griseb.), provides the possibility of subsequent absorption of nutrients released by decay of
any matter, whether plant or animal, that ends up
falling into these structures. Other plants appear to
be mining these same sort of veins, but are not
considered to be carnivores, although they certainly
could benefit from the decay of animals that happen
to be among the items they collect in either ‘trash
basket’ systems of roots (as in some orchids, including
species of Ansellia Lindl., Catasetum Rich. ex Kunth
and Grammatophyllum Blume) or sterile leaves (as in
the ferns Platycerium Desv. and Drynaria (Bory)
J.Sm.; Polypodiaceae).
The carnivorous syndrome in angiosperms has
largely been focused on the plants that are clearly
trapping, digesting and absorbing the resulting products, such as Drosera, Utricularia and Genlisea A.St.Hil., but many authors have noted that other species
may be going about the same business in a much less
obvious way. Darwin (1875) noted that many plants
have developed sticky glands that trap and kill
insects, such as Erica tetralix L., Mirabilis longiflora
L., Pelargonium zonale L’Hér., Primula sinensis Lour.
and Saxifraga umbrosa L., but no one has further
investigated these species to determine if something
more sinister is in fact taking place. Some of these,
such Erica tetralix, grow in nutrient-poor soils and
†As in the movie, Finding Nemo, about a clownfish that lives
in the tentacles of sea anemones without suffering from their
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
are members of families related to those of carnivores
(in this case, Sarraceniaceae), so they are likely candidates for investigation. Earlier in the 20th century,
several Italian researchers (Mameli, 1916; Mameli &
Aschieri, 1920; Zambelli, 1929; see discussion of these
papers by Simons, 1981) suggested that yet other
plants (Martynia L., Lychnis L. and Petunia Juss.,
respectively) with sticky leaves were in fact digesting
prey, although the experiments to support these
contentions were not particularly sophisticated and
today would be considered inconclusive.
In this part of our review, we focus upon (1) the
phylogenetic arrangement of the families that
most authors have thought to be carnivorous, (2)
the degree of modifications made to enable carnivory
(by describing the mechanisms by which prey are
trapped, killed and digested) and (3) the other genera
of plants that have been hypothesized by at least
some authors to be carnivorous and discuss the
evidence for this.
As stated above, Darwin assumed that some parallelisms were likely among trapping types. Tank-forming
plants such as the bromeliads Brocchinia and Catopsis aside (because they inherited the trapping structure from their ancestors and merely developed
greater absorptive capacities in order to become
carnivorous), pitcher plants evolved three times in
the angiosperms, in Nepenthaceae (Nepenthes) in
Caryophyllales, Cephalotaceae (Cephalotus Labill.) in
Oxalidales (a rosid order) and Sarraceniaceae (Darlingtonia DC., Heliamphora Benth. and Sarracenia)
in Ericales (an asterid order), whereas flypaper leaves
may have evolved at least five times: Droseraceae
(Drosera), Drosophyllaceae (Drosophyllum Link),
Dioncophyllaceae (Triphyophyllum Airy Shaw), all in
Caryophyllales, and Byblidaceae (Byblis Salisb.) and
Lentibulariaceae (Pinguicula L.), both in Lamiales
(an asterid order). Most authors would add Roridulaceae (Roridula) to this list, but, although the two
species of this genus clearly trap insects, they neither
digest nor absorb the released nutrients with specialized cells on their leaves (see below). There is an
equally parsimonious alternative to this because
three of these families are closely related; flypaper
traps may have evolved once in the common ancestor
of Droseraceae, Drosophyllaceae and Dioncophyllaceae, and then been lost in Ancistrocladus Wall. (the
sole genus of Ancistrocladaceae), Habropetalum Airy
Shaw and Dioncophyllum Baill. (the other two genera
of Dioncophyllaceae). Many other species exhibit
similar capacities to trap insects and other arthropods, so classifying Roridula as a carnivore is arbi-
trary. Snap traps probably evolved only once, in
Droseraceae in the common ancestor of Aldrovanda L.
and Dionaea Ellis (Cameron, Wurdack & Jobson,
2002). In Utricularia and Genlisea (Lentibulariaceae),
we find two novel types of traps, bladders under
pressure (formed on stolons, which are modified
stems) and spiralled tubular traps (formed by subterranean leaves), respectively; Pinguicula in the same
family has active flypaper traps.
Among angiosperms as a whole, flypaper traps are
by far the most numerous, and it is easiest to consider
a flypaper trap as the logical evolutionary antecedent
for the development of more specialized traps. Once
trapping/digesting of prey occurs, then further structural modifications/physiological developments to
improve its function or specialize in particular types of
prey are easier to envisage. In nearly all cases of other
specializations, flypaper traps occur among the related
genera, except in the case of Cephalotus (Cephalotaceae, Oxalidales), which is the most distantly related
species relative to the others known. Other families in
Oxalidales, for example, Cunoniaceae and Elaeocarpaceae, have mucilage secreting cells in their epidermis, and a few genera (e.g. Eucryphia Cav.,
Cunoniaceae) are glandular. In several other cases,
stalked secretory glands are common among other
families in orders with carnivorous taxa, for example,
Caryophyllales (Lledó et al., 1998) and Lamiales.
Below we provide an overview of known carnivorous
plants and their phylogenetic relationships, presented
in the order from APG III (2009). Considering that
there are varying degrees of carnivory exhibited by
many angiosperms, this list will not be exhaustive,
and good evidence for carnivory will most likely be
found in other plant groups in the future. For each
carnivorous genus, we provide habitat preferences,
mechanisms of trapping insects, glandular modifications to aid digestion and absorption of digestion
products and an assessment of their degree of active
Rosette-forming leaves of many bromeliads form
tanks, in which they catch rainwater, allowing them
to survive dry periods in the canopy of rainforests.
Roots of most bromeliads are non-absorptive and
function only to attach these plants to their substrate
or host plant (in the case of the epiphytic species).
Absorption by roots is replaced by absorption of min-
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
erals and potentially nutrients from their tanks via
specialized scale glands, and these have been documented to absorb labelled amino acids (reviewed in
Givnish et al., 1984). In these ‘pitchers’, whole ecosystems can develop, and they are an important breeding
ground for tree-dwelling frogs in tropical America, as
well as a source of nutrients for the epiphytic species
in particular.
Brocchinia reducta Baker, a terrestrial species
from southern Venezuela and Guyana, grows in
sunny, wet, nutrient-poor habitats alongside other
carnivores such as Heliamphora. This species has a
specialized ‘pitcher’ formed by the leaf rosette in
which water accumulates. The insides of the leaves
are covered in waxy scales that reflect ultraviolet
light, and many insects are attracted by this combination and lured into the trap. Brocchinia reducta
was originally thought not to produce enzymes, and
digestion was then considered to be performed by a
community of inquilines (Givnish et al., 1984). The
pH of the liquid in the pitcher of B. reducta measured 2.8–3.0, so this too would aid in breaking
down material that fell into the liquid. It is known
to contain large numbers of drowned insects and
has recently been demonstrated to produce phosphatases, albeit weakly (Płachno et al., 2006); thus,
it can be considered a carnivorous plant in the strict
sense. The trapped insects are broken down, and
the nutrients released are absorbed by the glandular leaf scales. A closely related species, B. hechtioides Mez, has also been considered to be similarly
carnivorous, but this species has not been studied so
far in detail (Givnish et al., 1997).
Similarly, Catopsis berteroniana (Schult. &
Schult.f.) Mez, an epiphytic species that can be found
from Florida to Brazil, appears to trap more insects
than other bromeliads of a similar size (Frank &
O’Meara, 1984). However, Givnish et al. (1984) performed a cost–benefit analysis, which showed that
only plants growing in wet, bright conditions would
be likely to make full-blown carnivory a successful
strategy. Epiphytic species should not be carnivorous,
but it is clear that some species growing in dry areas
can be carnivores (e.g. Drosophyllum, Drosophyllaceae, and some Drosera spp., Droseraceae; Caryophyllales, see below). Some Nepenthes spp. growing in
humid environments can effectively be epiphytes, and
many grow in a high degree of shade.
Most species of Puya Molina have extremely sharp,
outwardly pointing spines, probably to deter herbivores. In contrast, the spines of P. raimondii Harms
point inward towards the rosette. This tree-like
Andean bromeliad is bird pollinated, and several bird
species also use the rosette as a nest site, with the
inward pointing spines providing stability for the
nest. Some birds are also trapped by the spines and
killed. Rees & Roe (1978) counted a total of 44 dead
birds in only 17 plants. Because the leaves are curved
into a trough shape, it may allow P. raimondii to
benefit from the added nutrients provided by run-off
of accumulated nest debris and faeces, not to mention
dead birds.
Paepalanthus bromelioides Silv. shares the habitat of
Brocchinia reducta, and its leaves also form a tank
that may function in a similar fashion as that of
Brocchinia (Jolivet, 1998). This is, however, highly
speculative, and no study has been carried out on
possible trapping, digesting or absorbing mechanisms
of this species.
Darwin (1875) reported that peduncles and petioles of
Saxifraga umbrosa L. are clothed in pink glands that
secrete a yellowish viscid fluid, which can rarely
entrap minute Diptera. He proceeded to experiment
on flower stems in a manner similar to, although less
extensive than, his studies on Drosera. Dipping them
into infusions of raw meat, he noted movements in
the protoplasm ‘exactly like those described in the
case of Drosera.’ With exposure to solutions of ammonium carbonate, he observed that ‘there is the closest
resemblance to what takes place when a tentacle of
Drosera is immersed in a weak solution of the same
salt. The glands, however, absorb very much more
slowly than those of Drosera.’ He concluded that more
evidence was necessary ‘before we can fully admit
that the glands of this saxifrage can absorb . . . animal matter from the minute insects which they occasionally and accidentally capture.’ For Saxifraga
rotundifolia L., he observed that the glands were able
to absorb ammonium carbonate much more quickly
than those of S. umbrosa. Darwin stated that ‘The
most interesting case for us [among the plants with
glandular hairs that he studied] is that of the two
species of Saxifraga, as this genus is distantly allied
to Drosera’. Although, molecular phylogenetic studies
have refuted this last statement, it appears that at
least some species of Saxifraga have glands that are
capable of trapping insects and that these same
glands can absorb a range of substances. The exudates from the glands have not been demonstrated to
have digestive properties, however, and it is unlikely
that these plants are true carnivores. Their habitat
preferences also do not appear to be those associated
with the classic cases of carnivory.
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
Figure 4. A, Cephalotus follicularis Labill., RBG Kew. B, Passiflora foetida L., showing flower with glandular bracts,
Punaauia, Tahiti. C, Dionaea muscipula Ellis ex L., active traps, Carolina Beach State Park, North Carolina. D, Drosera
pulchella Lehm., with winged petioles, cultivated at RBG Kew. E, Drosera regia Stephens, regular circination of unfolding
leaf, cultivated at RBG Kew. F, Drosophyllum lusitanicum (L.) Link, reverse circination of unfolding leaf, RBG Kew. All
photographs taken by Maarten J. M. Christenhusz.
Cephalotaceae are monotypic, the sole species being
Cephalotus follicularis Labill. (Fig. 4A), which is only
found in southwestern Western Australia. Generally
known as the Albany pitcher plant, it is also sometimes referred to as the moccasin plant or Western
Australian or (historically) New Holland pitcher
plant. Described by Labillardière on the basis of
material that has apparently been lost (Willis, 1965),
further details of the taxonomic history of this species
are given by McPherson (2009). Although described in
1806, it appears to have been unknown to Darwin
and is not mentioned in his book, although he did
visit Western Australia, which left him famously
Passiflora L. is known for its glands that mimic insect
eggs to fool especially butterflies that do not lay eggs
if there are already some present on leaves. Similarly,
the peculiar, pantropical, weedy passion flower, Passiflora foetida L., has long glandular hairs on the
bracts subtending its white–green flowers (Fig. 4B).
These multicellular, stalked glands that are remarkably similar to those of taxa in Caryophyllales have
been proven to produce digestive enzymes (Radhamani, Sudarshana & Krishnan, 1995), suggesting
insects get trapped in the fine netting of the bracts
and are digested. However, there is no mention of
sterilizing the bract surface or otherwise demonstrating that production was endogenous, nor was absorption definitively demonstrated. This may simply be
another case of a sticky floral defence against herbivory. It does not fit the syndrome of habitat features
observed in other carnivorous taxa (Givnish et al.,
1984); P. foetida inhabits wet tropical areas in which
carnivores are otherwise absent. It is also an invasive
in tropical ruderal zones worldwide.
FEBRUARY 17TH. – The Beagle sailed from Tasmania, and,
on the 6th of the ensuing month, reached King George’s
Sound, situated near the S.W. corner of Australia. We staid
there eight days; and I do not remember, since leaving
England, having passed a more dull, uninteresting time.
(Darwin, 1839)
Although the pitchers are superficially similar to
those of Nepenthes, Brown (1832) stated that the two
genera ‘differentiate in so many other important
characters that they cannot be considered as nearly
related.’ Among other characters, Cephalotus Labill.
differs from Nepenthes in its hermaphrodite flowers.
Like Nepenthes, however, Cephalotus produces its
own digestive enzymes and is thus an active carnivore (see McPherson, 2009 for further details). It also
grows in wet, sunny sites where other carnivorous
taxa are common, particularly Drosera spp., including
the enormous D. gigantea Lindl. Phylogenetic studies
indicate that Cephalotaceae belong to Oxalidales,
within which they are related to Brunellia Ruiz &
Pav. (Brunelliaceae) and then to Eleaocarpaceae and
Cunoniaceae; Cephalotus folicullaris is thus only distantly related to any other carnivorous taxa (APG III,
2009) and unusual in belonging to a clade in which
glands are not always present. Mucilage-producing
epidermal cells or hairs (some genera of Elaeocarpaceae and Eucryphia, Cunoniaceae) do occur in the
families of Oxalidales and evidently can serve as
antecedents for development of the digestive and
absorptive glands in Cephalotus.
Many members of Rosaceae are covered with glandular, often sticky, processes. Insects often become
entrapped, and it has widely been assumed that
these glands have a defensive capability. However,
members of the Potentilla arguta Pursh complex
(sometimes placed in Drymocallis Fourr. ex Rydb.,
including also P. glandulosa Lindl. and P. rupestris L.)
appear capable of not only trapping insects, but also
digesting them and absorbing the released nutrients
(Spomer, 1999). These species occur in habitats that
can support other carnivores, especially Drosera, and
fit the syndrome of conditions associated with carnivory, but Spomer (1999) admitted that he could not
rule out surface microbes as the source of the
enzymes he observed to be digesting insects trapped
by the hairs on these species of Potentilla.
As in the case for Potentilla (Rosaceae; see above),
Spomer demonstrated that Geranium viscosissimum
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
Fisch. ex C.A.May has the potential to be carnivorous.
It appears to secrete digestive enzymes and be capable
of absorbing amino acids. As for P. arguta, it cannot be
ruled out that surface microbes are responsible for
digestion, but, in the same series of experiments,
leaves of Petunia did not exhibit this activity, so either
the microbes responsible do not occur on Petunia or the
enzymes are released only by G. viscossisimum. The
habitat preferences for this species (moist roadsides
and creek banks, sometimes in shade) do not seem to
be clearly those associated with the carnivorous syndrome, and no other carnivorous taxa grow with it.
Darwin (1875) also mentioned possible carnivory associated with the glandular hairs on Pelargonium zonale
L’Hér., but no one has ever investigated this further. As
for G. viscossisimum, this seems an unlikely carnivore,
given its habitat preferences.
Carnivorous seeds are perhaps a strange concept, but
tests have been carried out on the seeds of shepherd’s
purse, Capsella bursa-pastoris Medik. (Barber, 1978).
It was shown that the mucilage layer of seeds upon
imbibition contains chemicals that attract soil nematodes, protozoa and soil bacteria and a toxin that kills
these organisms. The mucilage also produces proteinases and labelled amino acids were found to be taken
up by the seeds. It is easy to imagine that seedlings
would benefit nutritionally from the breakdown of
these organisms.
Various members of the genera Lychnis and Silene L.
have sticky hairs and are known by the common
name of ‘catchfly’. Despite this, most modern authors
have given little credence to them being carnivorous.
Barthlott et al. (2007), for example, reported that
Lychnis viscaria L. is one of the non-carnivorous
plants that ‘have developed sticky leaves as a defense
against feeding insects’ (along with Nicotiana
tabacum L. and Passiflora foetida), but continued that
the insects thus trapped ‘are not digested because
these plants have no digestive enzymes’. However,
Mameli & Aschieri (1920) demonstrated that L. viscaria ‘without doubt contains a proteolytic enzyme,
that renders the proteinous substances slowly soluble’
and that ‘the viscous zones of the stalks of the plants
are permeable’. Spomer (1999) demonstrated that the
sticky exudates of some other members of Caryophyllaceae (Cerastium arvense L. and Stellaria americana
(Porter) Stanl. and S. jamesiana Torr.) showed protease activity, but he did not investigate uptake of the
products of digestion. Further research would be necessary to demonstrate full carnivory in this family.
Dioncophyllaceae consist of three monotypic genera,
Dioncophyllum Baillon, Habropetalum Airy Shaw
and Triphyophyllum Airy Shaw, all lianas or shrubs
endemic to tropical West Africa. Molecular studies
(e.g. Fay et al., 1997; Cameron et al., 2002; Cuénoud
et al., 2002; Heubl, Bringmann & Meimberg, 2006)
have shown them to be most closely related to Ancistrocladaceae, with a single genus Ancistrocladus
Wallich consisting of 12 species of lianas in tropical
Africa and Indomalaysia. This pair of families is most
closely related to Drosophyllaceae and then more
distantly to Droseraceae, Nepenthaceae and other
caryophyllalean families.
Green, Green & Heslop-Harrison (1979) demonstrated that Triphyophyllum peltatum (Hutch. &
Dalziel) Airy Shaw is carnivorous. The other two
genera of Dioncophyllaceae and Ancistrocladus lack
the carnivorous habit. Dioncophyllum appears to be
eglandular, and the glands in Habropetalum are
simple and present only on young stems. This lack of
carnivory probably represents losses in these three
genera, given the relationship to Drosophyllaceae and
other carnivorous plant families (e.g. Heubl et al.,
Triphyophyllum is heterophyllous, producing three
types of leaves, two generally found on non-climbing,
juvenile shoots and the third on adult climbing shoots.
Short shoots firstly produce mostly eglandular oblanceolate leaves (Fig. 5A), but, just before the height of
the rainy season, glandular filiform leaves (Fig. 5B)
are produced, which are relatively short-lived, surviving for only a few weeks. As in Drosophyllum, these
show reverse circinnation. The glandular leaves bear
stalked and sessile glands (Fig. 5C) and are efficient in
trapping prey (Fig. 5B; mostly insects, with Coleoptera
being the most common). Large numbers of prey are
trapped: Green et al. (1979) found c. 21 identifiable
carcases per leaf plus other chitinous remains. Occasional leaves intermediate in form between these two
types are found on the juvenile shoots (see for example
McPherson, 2008). The leaves of the mature axis are
oblanceolate and have apical hooks (Fig. 5D), enabling
the liana to climb into the canopy. The account of
Triphyophyllum by McPherson (2008) included many
more photographs illustrating the different leaf types
and other features, including the prominently winged
pink seeds.
The glandular leaves possess stalked and sessile
glands. The stalked glands fall into two size classes
(2–3 mm and c. 1 mm) and bear secretion droplets
that trap prey. The sessile glands are dry until
stimulated. The gland stalks are vascularized, as in
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
Figure 5. Triphyophyllum peltatum (Hutch. & Dalziel) Airy Shaw. A, eglandular leaves on juvenile shoots. B, glandular
leaves on a juvenile shoot. C, close-up of glandular leaf showing two types of glands. D, mature axis with grappling hooks.
Photographs taken by Stewart McPherson (2008).
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
Drosera and Drosophyllum, and also in Passifloraceae
(including Turneraceae), but this condition is otherwise unknown in the angiosperms. Green et al. (1979)
stated that the stalked glands are ‘the most anatomically elaborate known in the plant kingdom’. They
also demonstrated that the secretions of these glands
contain proteases and other enzymes.
Juniper, Robins & Joel (1989) referred to Triphyophyllum as the ‘part-time carnivorous plant’. It is
unusual among carnivores in being well rooted and
has only a transient carnivorous phase. Green et al.
(1979) reported that there is evidence that Triphyophyllum leaves are relatively rich in potassium,
which is deficient in the surrounding soil, and they
wrote ‘It seems possible that the transition from the
juvenile phase requires that some threshold level
should be reached in nutrient reserves, and in the
absence of adequate soil resources carnivory could be
the means for gaining this threshold more rapidly.’
They continued ‘The limited growth of the short shoot
is accompanied by an alternation of groups of longlasting photosynthetic leaves and shorter-lived insectcapturing leaves. This growth pattern might be
expected to permit the hoarding of nutrients until the
moment was reached when a switch could be made to
the development of the rapidly growing, efficiently
climbing liane.’ More recent studies in the field by
McPherson (2008), however, indicated that plants are
able to switch between primary and secondary foliage
types more than once in their life cycle.
Carnivory appears to be well established in the case
of Triphyophyllum, although it grows in rather atypical shady environments, not generally associated with
carnivorous plants (Juniper et al., 1989). Green et al.
(1979) suggested that a parallel with Triphyophyllum
may be seen in epiphytic and climbing Nepenthes,
although the ability of Triphyophyllum to grow in
shade and the lack of carnivory shown by the leaves
of the mature liana clearly distinguish it from
members of that genus.
Droseraceae comprise three genera, Aldrovanda,
Dionaea and Drosera. Aldrovanda (one species) is a
widespread aquatic in the Old World, and Dionaea
(also a single species) is endemic to a small swampy
area in North and South Carolina. Drosera (more
than 180 species), in contrast, is extremely widespread, occurring on all continents except Antarctica.
Notable radiations occur in Australia and South
Africa. Although Darwin (1875) considered Droseraceae to include six genera (Aldrovanda, Byblis,
Dionaea, Drosera, Drosophyllum and Roridula), phylogenetic studies have demonstrated that Byblis,
Drosophyllum and Roridula should be excluded, with
Drosophyllum being more closely related to the other
caryophyllalean families (Ancistrocladaceae, Dioncophyllaceae and Nepenthaceae) and Byblis and
Roridula being members of Lamiales and Ericales,
respectively. In spite of this narrowing of their circumscription, Droseraceae nevertheless demonstrate
remarkable diversity in morphology, specifically in
their mode of carnivory, with two major forms of
traps: flypaper traps in Drosera and snap traps in
Aldrovanda (Fig. 6) and Dionaea (Fig. 4C). Cameron
et al. (2002) showed that Aldrovanda is sister to
Dionaea and this pair is sister to Drosera (Fig. 4D, E),
but with relatively weak support for this pattern of
In analyses using rbcL sequence data alone, Rivadavia et al. (2003) with greater species sampling
placed Aldrovanda as sister to D. regia (Fig. 4E), but
with no support for these relationships. In their
analyses of rbcL in combination with sequences of
18S nuclear ribosomal DNA, however, they recovered
a weakly supported monophyletic Drosera, and Aldrovanda was moderately supported as sister to Dionaea.
Heslop-Harrison (1976) referred to the traps of
Drosera as being passive and those of the other two
genera as active, although the power of movement
demonstrated by Darwin (1875) in Drosera leaves
indicates that these are also active, if somewhat
slower in their response.
Darwin (1875) devoted the great part of his book on
carnivorous plants to a series of experiments on
Drosera, the first ten chapters (out of 18) dealing
almost exclusively with Drosera rotundifolia L.
(Fig. 7), the common sundew, the eleventh summarizing the previous ten chapters and the twelfth detailing observations on other species of Drosera. Chapters
13 and 14 cover his observations on Dionaea muscipula and Aldrovanda vesiculosa L., respectively.
Through his work on D. rotundifolia, Darwin demonstrated that the ‘tentacles’ are capable of rapid
movement in response to stimuli (beginning after as
little as 10 seconds), the glands are absorptive and
that stimulating one tentacle caused movement in
the surrounding tentacles (Chapter 1). In Chapter 2,
he showed that animal substances caused a much
quicker and stronger response than inorganic substances or mechanical irritation and that movement
only occurred if a tentacle was touched briefly three
or more times. In Chapter 3, he described the process
of aggregation of cellular contents in the glands after
excitation. Chapter 4 deals with the effects of immersion in water at different temperatures and Chapter 5
with the effect of nitrogenous and non-nitrogenous
organic fluids (comparing, for example, the effects of
decoctions of green peas or cabbage with infusions
of raw meat). In Chapter 6, Darwin described the
experiments by which he demonstrated that ‘the
leaves are capable of true digestion, and that
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
Figure 6. Aldrovanda vesiculosa L. (from Insectivorous Plants, Darwin, 1875: fig. 13).
the glands absorb the digested matter’, stating that
‘These are, perhaps, the most interesting of all my
observations on Drosera, as no such power was before
distinctly known to exist in the vegetable kingdom’.
Through these experiments he demonstrated that the
enzymatic action was not active in untouched leaves
and that ‘the ferment of Drosera is closely analogous
to, or identical with, the pepsin of animals’. Observations on the effects of ammonium salts, other salts
and acids and ‘alkoid poisons, other substances and
vapours’ are presented in Chapters 7–9, and the
nature of the sensitiveness of leaves and transmission
of the motor impulse are discussed in Chapter 10.
Although the trapping mechanism of all Drosera
spp. is basically the same, vegetative morphology of
the plants varies greatly between species. Many are
rosette forming, but an extreme variation is found in
D. gigantea Lindl. in southwestern Australia, which is
c. 1 m tall and produces annual growths with many
flypaper traps on a highly branched, erect, selfsupporting stem.
Dionaea muscipula is one of the best-known carnivorous plants, and it has been demonstrated to
show all parts of the carnivorous syndrome. The trap
mechanism (with its trigger hairs) and enzyme secretion have been studied in detail (e.g. Darwin, 1875;
Heslop-Harrison, 1976; Cameron et al., 2002; Forterre
et al., 2005; Płachno et al., 2006). When the trigger
hairs are stimulated, a current is generated by
calcium ions, the change in acidity makes the midrib
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
Figure 7. Drosera rotundifolia L. (from Insectivorous Plants, Darwin, 1875: fig. 1).
cells change shape as a result of osmosis and the trap
closes. After several days the prey is reduced to its
chitin skeleton, and the trap reopens for reuse.
The popularity of Venus’ fly traps in cultivation and
the limited area of distribution in the Carolina swamps
has resulted in a great threat to the native populations. Currently wild plants are protected, and wild
collections are illegal. Nevertheless, the sites are
under threat from urban development, and the species
is therefore classified as ‘vulnerable’ (IUCN, 2009).
Dionaea muscipula has been introduced to swamps in
Florida, New Jersey, California and Jamaica, where
populations have become well established.
Despite the difference in their habitat, the traps of
Aldrovanda bear clear similarity to those of Dionaea
(e.g. Juniper et al., 1989), albeit somewhat miniaturized, and function in a similar way. Darwin (1875)
described Aldrovanda as ‘a miniature, aquatic
Dionaea’, and Cameron et al. (2002) stated that ‘it is
not difficult to envision a Dionaea-like, terrestrial
ancestor of Aldrovanda vesiculosa becoming adapted
to a permanently aquatic lifestyle’.
Darwin’s fascination with carnivorous plants carried
forward into his studies of the power of movement in
plants (Darwin, 1880), with observations on Dionaea,
Drosera and Sarracenia. With reference to altered
behaviour because of carnivory, he stated that:
Heliotropism prevails so extensively among the higher plants,
that there are extremely few, of which some part, either the
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
stem, flower-peduncle, petiole, or leaf, does not bend towards
a lateral light. Drosera rotundifolia is one of the few plants
the leaves of which exhibit no trace of heliotropism. Nor could
we see any in Dionaea, though the plants were not so carefully
observed. Sir J. Hooker exposed the pitchers of Sarracenia for
some time to a lateral light, but they did not bend towards it.
We can understand the reason why these insectivorous plants
should not be heliotropic, as they do not live chiefly by decomposing carbonic acid; and it is much more important to them
that their leaves should occupy the best position for capturing
insects, than that they should be fully exposed to the light.
Drosophyllaceae include one species, Drosophyllum
lusitanicum (L.) Link (Fig. 4F), native to the Iberian
Peninsula (Atlantic coast of Portugal, the southernmost tip of Spain and Gibraltar) and northern Africa
(northernmost Morocco). Its common names are Portuguese sundew and dewy pine. It is unusual among
carnivorous taxa in that it grows in dry basic rather
than wet acidic soils, but the sites it inhabits are
nonetheless nutrient deficient. No other carnivorous
taxa grow in these habitats. It was originally
described as a species of Drosera by Linnaeus in
Species Plantarum (Linnaeus, 1753), and it does
resemble the species of that genus, except for its
reversely circinnate leaves (Fig. 4F; compare with
Fig. 4E) that do not move when capturing prey. It
forms an often stalked rosette of leaves covered with
sticky, mucilage-secreting, long glands that trap prey
(flypaper traps); plants reach approximately 40 cm
in height. Once trapped, insects are dissolved by
enzymes released by short glands on the leaves, and
the released nutrients are absorbed by the plant. It is
thus an active carnivore because it has all the cellular
mechanisms to trap prey, digest them and absorb
nutrients. Molecular phylogenetic studies have demonstrated that Drosophyllum is more closely related
to Dioncophyllaceae (see above), Ancistrocladaceae
(not carnivorous) and probably Nepenthaceae than it
is to Droseraceae (all Caryophyllales; Fay et al., 1997;
Cuénoud et al., 2002). It was known to Darwin, who
drew sketches of the two types of glands on its leaves.
Nepenthaceae include only one genus, Nepenthes L.,
and the most recent major treatment lists 120 species
and five ‘incompletely diagnosed taxa’ (McPherson,
2009). The author of this work stated that
I have prepared this two volume work to provide a visually
rich overview of the biology, ecology, diversity, distribution and
conservation status of Nepenthes and Cephalotus. This work is
not intended as a botanical or taxonomic monograph
and referred readers to a number of ‘appropriate
printed sources’ for more detailed taxonomic treat-
ments. Despite this disclaimer, this work (reviewed by
Fay, 2009) represents the most complete work published in recent years, and the other works cited are
regional treatments. The short account below is
largely based on that of McPherson (2009).
Nepenthes is native to a large part of the Old World
Palaeotropics (but not Africa), with the vast majority
of the species occurring on the Sunda Shelf in southeastern Asia. Borneo, Sumatra, Sulawesi and the
Philippines are home to notable radiations of species.
Madagascar, the Seychelles, Sri Lanka, northern
India, Papua New Guinea, northeastern Australia,
New Caledonia and some isolated Pacific islands are
home to small numbers of species. Nepenthes species
generally grow in thin mats of leached organic
matter, which can overlay alkaline, neutral or acid
Although known from Madagascar since the 17th
century, Linnaeus (1753) based his description of
Nepenthes on material from Sri Lanka, with a single
species, N. distillatoria L. Common names are tropical or Asian pitcher plants and, for some species,
monkey pots. McPherson (2009) listed a wide range of
common names in other languages.
Seedlings of Nepenthes form rosettes and, in the
majority of species, plants then form a scrambling or
climbing stem. The traps of Nepenthes are pitchers
(Fig. 8) formed from tendrils [similar in development
to the grappling hooks in Triphyophyllum (Dioncophyllaceae; see above)]. All leaves can bear tendrils or
pitchers and, when growing conditions are not ideal,
the tendrils fail to develop into pitchers. The pitchers
are borne on the end of tendrils of variable length
(Fig. 9A) and are hollow vessels with a mouth into
which prey can fall. The size of the pitchers varies
between species from only a few centimetres in length
to > 30 cm, and they can hold three or more litres (for
more details about the morphology of Nepenthes, see
McPherson, 2009).
The pitchers are (at least in part) lined with secretory glands that produce the digestive liquid, and the
upper part of the interior of the pitcher is generally
smooth and waxy. The digestive process is thought to
be partly because of the enzymes secreted in the
liquid in the pitchers and partly because of microorganisms in the liquid. In newly opened pitchers, the
liquid can be highly acidic (pH 2.5; Heslop-Harrison,
1976). Nepenthes species are thus active carnivores
because they trap prey, digest them and absorb nutrients. This active carnivory was already known in the
19th century. In his sole reference to Nepenthes,
Darwin (1875) reported that:
Dr Hooker likewise found that, although the fluid within the
pitchers of Nepenthes possesses extraordinary power of digestion, yet when removed from the pitchers before they have
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
Figure 8. Nepenthes eymae Shigeo Kurata, cultivated at RBG Kew. Photograph taken by Maarten J. M. Christenhusz.
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
been excited and placed in a vessel, it has no such power,
although it is already acid; and we can account for this fact
only on the supposition that the proper ferment [enzyme] is
not secreted until some exciting matter is absorbed.
Prey items are predominantly invertebrates,
although occasional cases of the remains of amphibians and even small mammals being found in pitchers
have been reported. Specialisation on particular types
of prey has been reported (Moran et al., 2001), and
some species appear to have forgone carnivory altogether. In addition to prey items, pitchers of Nepenthes can provide a home for various micro-organisms,
invertebrates and even vertebrates, which may take
advantage of the trapping of other animals by the
plants (see McPherson, 2009 for extensive review of
the fauna of Nepenthes pitchers).
Darwin (1875) reported that the stems and leaves
of Mirabilis longiflora bear viscid hairs, and young
plants ‘caught so many minute Diptera, Coleoptera,
and larvae, that they were quite dusted with them’.
On the basis of experiments with ammonium carbonate and infusions of meat he concluded, however, that
the glands on these hairs had no power of absorption.
His final words on the subject were:
We may further infer that the innumerable insects caught by
this plant are of no more service to it than are those which
adhere to the deciduous and sticky scales of the leaf-buds of
the horse-chestnut [Aesculus hippocastanum L.].
Claims that the seeds of Pisonia grandis R.Br. trap
and kill seabirds for the added nutritional benefit of
germinating near a decomposing corpse were investigated by Burger (2005). His study was based on
numerous reports of dead birds that apparently died
after being entangled in the sticky infructescences of
this coastal tree species. Burger found that any
possible benefit to the germinating plants was outweighed by damage caused by scavenging crabs that
were attracted to the decomposing birds. The killing
of birds by P. grandis seeds, however morbid, seems
more an adaptation to distribute seeds effectively to
various oceanic islands than an actual adaptation for
Like Passiflora foetida, species of leadwort, Plumbago
L., have sticky, multi-celled, vascularized, glandular
hairs in the inflorescence that capture many insects.
Plumbago capensis Thunb. has been suggested to be
carnivorous, but no evidence for protease and uptake
was shown (Rachmilevitz & Joel, 1976). The glands
are only produced in the inflorescence and are probably more of a defence mechanism against herbivory
or a means to attach seeds to animals, aiding in their
dispersal. If at all carnivorous, Plumbago shows a
passive form of proto-carnivory.
Although Darwin (1875) mentioned the possibility
that Erica tetralix could be carnivorous because of it
having glandular hairs that secrete ‘viscid matter’
and occasionally catch minute insects, he showed that
the glands have little or no power of absorption. We
are not aware of any further publications providing
evidence of carnivory in this species.
In Primula sinensis Lour., the flower stems, leaves
and petioles are clothed in longer and shorter hairs,
and the longer hairs have an enlarged terminal cell,
forming a gland which secretes a variable amount
of thick, slightly viscid, not acid, brownish–yellow
matter. Exposure to solutions and vapours of ammonium carbonate led Darwin (1875) to state that ‘in
both cases there could hardly be a doubt that the salt
had been absorbed chiefly or exclusively by the
glands’. Weak infusions of meat, however, had no
effect. Thus, although the glands appear to be capable
of absorption of some material, there is no evidence
for uptake of nutrients or digestion.
The single genus in this family Roridula consists of
two species of South African subshrubs, R. dentata L.
and R. gorgonias Planch. The leaves resemble those of
Drosera in being covered in long glandular hairs and
excrete a sticky sap that traps insects (Fig. 9B).
Despite its morphological resemblance to sundews,
they lack the specialized absorptive glands on the
leaves that other carnivorous plants have, permitting
the uptake of dissolved prey, suggesting that this is not
a fully carnivorous species. However, two species of
hemipteran, Pameridea roridulae and P. marthothii,
are closely associated with Roridula, living their entire
lives on these plants (Dolling & Palmer, 1991) without
getting trapped. It was initially thought that these
bugs intercepted the nutrients within trapped prey
before it could be absorbed by the plant. Ellis &
Midgley (1996) studied this relationship further and
found that the faeces of Pameridea played an important role. This was the first account of a mutualist
relationship between a carnivorous plant and an
insect, in which Pameridia benefited from the trapped
prey and Roridula benefited from the indirect digestion of nutrients. Anderson (2005) investigated the
method of absorption in Roridula and found absorption
through unusual cuticular gaps, which is most likely
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
Figure 9. A, Nepenthes sp., unfolding pitcher at the tip of a climbing tendril, cultivated at RBG Kew. B, Roridula
gorgonias Planch. with a trapped bluebottle (Calliphora vomitoria L.), cultivated at RBG Kew. C, Sarracenia flava L.,
Carolina Beach State Park, North Carolina. D, Byblis liniflora Salisb., showing the glands, cultivated at RBG Kew. E,
Byblis gigantea Lindl., habit, near Perth, Western Australia. F, Proboscidea louisianica Thell., Turku Botanical Garden,
Finland. Photographs A–D and F taken by Maarten J. M. Christenhusz. Photograph E taken by Michael F. Fay.
the way the nutrients from the Pameridia faeces are
absorbed by Roridula.
The population density of Pameridia on plants of
Roridula is negatively correlated with the density of
the spider Synaema marlothi, a species that feeds
on both trapped prey and Pameridia (Anderson &
Midgley, 2002). Pameridia also sucks the sap from
Roridula, and this herbivory reduces the benefit of
the nutrients when the population of Pameridia
becomes too large. Synaema marlothii is important in
this mutualistic triangle to stabilize the populations
of Pameridia and maintain the balance (Anderson &
Midgley, 2007).
Sarraceniaceae include three genera distributed
mostly in North America (Sarracenia L., with c. 11
species in eastern and northern North America and the
monotypic Darlingtonia Torr. in the far west) with a
disjunct distribution in northern South America (Heliamphora Benth., Fig. 10, with more than 15 species,
and more being described as additional tabletop mountains, tepuis, are investigated). The plants of all three
genera grow in nutrient-poor, acid bogs, and only the
species of Sarracenia are full-fledged carnivores,
exhibiting wax scales on the upper surfaces that
increase the chances that an insect will lose its footing
and fall into the pitcher, which produces digestive
enzymes and absorbs the released nutrients. Heliamphora tatei Gleason, which is also unusual in the
otherwise herbaceous family in being a shrub (up to
4 m tall), has also been found to have wax scales and
produce digestive enzymes (Jaffe et al., 1992), so complete carnivores do exist in Sarrraceniaceae outside
Sarracenia. Some species of Sarracenia also produce
nectar around the rim of the opening (reputed to
contain coniine, a narcotic, in S. flava L.; Fig. 9C, and
nectar production appears to be more important in
attracting prey than does the colour of pitchers
(Bennett & Ellison, 2009; Schaefer & Ruxton, 2008)).
Darlingtonia, like most species of Heliamphora, is a
passive carnivore and depends on bacteria in the
pitcher to digest prey, which it then absorbs.
In terms of phylogenetic relationships, Heliamphora and Sarracenia are sister taxa, with Darlingtonia sister to this pair (Bayer, Hufford & Soltis,
1996). This makes the biogeographical relationships
more difficult to explain, most authors having hypothesized a South American origin for the family
(Maguire, 1970; Juniper et al., 1989), and suggests
that Darlingtonia has been an isolated taxon for a
relatively long time. Some authors had also thought
that Heliamphora was the most primitive morphologically, but this does not immediately mean that it
should be sister to the other two genera. In any case,
most features of Sarraceniaceae do not occur in any of
the outgroup taxa, including Roridula, which most
analyses have placed as sister to Sarraceniaceae
(Albert et al., 1992; Chase et al., 1993) making polarization of morphological characters problematic.
[See Droseraceae, above, for discussion of lack of
heliotropism in Sarracenia (Darwin, 1880).]
Saccifolium bandeirae Maguire & J.M.Pires, often
treated as the sole member of Saccifoliaceae, has been
shown to be a member of Gentianaceae by Struwe
et al. (1998) and Thiv et al. (1999). This species has
strange pouch-like leaves, leading to suggestions that
it might be carnivorous, but with no convincing
evidence having been presented. Struwe et al. (1998)
discussed the possibility of it being a ‘carnivorous
gentian’, concluding that its position in the asterids
made this a possibility, but they then indicated that
further research to demonstrate digestion and absorption would be necessary. The opening to the leaves
is, however, downward facing, so it seems highly
unlikely that the pouches could be effective trapping
Long thought to comprise two species (Fig. 9D, E)
endemic to Western Australia (although the first
known collection was made in Queensland by Joseph
Banks et al. during Captain Cook’s first visit to Australia in 1770; McPherson, 2008), Byblidaceae now
consist of seven species in the genus Byblis. Of these,
two are perennial, occurring in Western Australia
near Perth, and five are annuals distributed across
tropical northern parts of Australia, with one species
also occurring on New Guinea (McPherson, 2008).
The superficial resemblance of Byblis to Drosophyllum led many to treat them as related, particularly
as the petals appear to be free. Close inspection,
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
Figure 10. Heliamphora nutans Benth., cultivated at RBG Kew. Photograph taken by Maarten J. M. Christenhusz.
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
however, reveals that the petals of Byblis are basally
fused (e.g. Lloyd, 1942). Phylogenetic studies have
indicated placement in Lamiales, although with no
strong support for interfamilial relationships within
that order (e.g. Müller et al., 2004, 2006).
Darwin (1875), on the basis of a dried specimen of
Byblis gigantea Lindl. (Fig. 9E) sent from Kew, noted
two forms of glands on the leaves, ‘sessile ones
arranged in rows, and others supported on moderately long pedicels’. The latter type were
far more simple in structure than the so-called tentacles of the
preceding genera [of Droseraceae in the broad sense, i.e.
Aldrovanda, Dionaea, Drosera, Drosophyllum], and they do
not differ essentially from those borne by innumerable other
plants. . . . As no instance is known of unicellular structures
having any power of movement, Byblis, no doubt, catches
insects solely by the aid of its viscid secretion. These probably
sink down besmeared with the secretion and rest on the small
sessile glands, which, if we may judge by the analogy of
Drosophyllum, then pour fourth [sic] their secretion and afterwards absorb the digested matter.
Darwin appears to have been more or less convinced that B. gigantea was carnivorous, although he
was unable to carry out his normal range of experiments to verify digestion and absorption because of
the lack of living material at his disposal. Elsewhere
in the book, he stated that:
There can hardly be a doubt that all the plants belonging to
these six genera have the power of dissolving animal matter
by the aid of their secretion, which contains an acid, together
with a ferment almost identical in nature with pepsin; and
that they afterwards absorb the matter thus digested. This is
certainly the case with Drosera, Drosophyllum, and Dionaea;
almost certainly with Aldrovanda and, from analogy, very
probable with Roridula and Byblis.
Bruce (1905) demonstrated that the sessile glands
(but not the stalked glands) had the power to digest
egg albumen, although Lloyd (1942) was unable to
demonstrate digestion of fibrin. Hartmeyer (1997,
1998) was not able to demonstrate enzyme production
by sessile glands of B. liniflora, but more recent
studies have shown that they produce enzymes
in B. filifolia (Hartmeyer & Hartmeyer, 2005) and
B. liniflora (Płachno et al., 2006; Fig. 9D).
Like Roridula, Byblis has been reported to have
potentially mutualistic relationships with various
arthropods and that at least some insects appear to
be able to move over the surface of the plant without
becoming entangled in the mucilage (Lloyd, 1942;
McPherson, 2008). However, the dynamics of these
relationships are not well understood.
Lentibulariaceae consist of three genera: Utricularia
(bladderworts; Fig. 2) that is sister to Pinguicula
(butterworts; Fig. 11), and Genlisea, which is sister to
this pair of genera (Müller et al., 2006). Utricularia
and Pinguicula have a more or less cosmopolitan
distribution; Genlisea is only found in tropical
America, Africa and Madagascar.
The morphologically variable genus Utricularia
consists of approximately 200 species and occurs
nearly worldwide. It is especially diverse in the
tropics, where species grow as aquatics, terrestrials,
epiphytes and even vines. In many species, there
are no clear distinctions between the roots, stems
and leaves. Epiphytes (such as the Antillean U.
alpina Jacq.) bear succulent tubers that contain
water. In the North Temperate aquatic bladderworts, roots are absent, even in seedlings. The
stems bear appendages that form bladder-like structures with trapdoors (Fig. 2). When a trapdoor
trigger is touched by a small animal, the trap opens
abruptly, and the animal is sucked into the bladder;
the trapdoor then re-closes, and the bladder secretes
enzymes and absorbs the products of digestion.
Aquatic species form bladders on photosynthetic
branches, and terrestrial species have their bladders
on achlorophyllous runners. The traps can range in
size from 0.2 mm to 1.2 cm (Taylor, 1989). Aquatic
species possess bladders that are usually at the
larger limit and can feed on more substantial prey,
such as water fleas (Daphnia), nematodes, fish fry,
mosquito larvae and even young tadpoles. Many
species have chasmogamous and cleistogamous
flowers in certain seasons and form buds to survive
dry periods or winters. Adamec (2007) demonstrated
low (approaching zero) partial pressures of oxygen
in traps of Utricularia and Genlisea and hypothesised that the prey may, at least in part, die of
anoxia. Sirová et al. (2009) showed that substantial
proportions of newly fixed carbon are exuded into
the trap fluid, possibly as a source of nutrients for
the microbial community living there.
Utricularia humboldtii Schomb. is peculiar in that
it is only found in the water tanks of Brocchinia
spp. (Bromeliaceae) at high elevations. The Australian U. multifida R.Br. and U. tenella R.Br. were
previously placed in the genus Polypompholix
Lehm., based on a somewhat different shape of the
trapping bladders. Molecular studies have, however,
shown that this and another segregate genus, Biovularia Kamieński, are embedded in Utricularia
(Jobson et al., 2003).
Pinguicula is named for its leaves that are greasy
to the touch; pinguis meaning fat in Latin. The
English common name butterwort results either from
the juice being used on the udders of cows (either
against magic or to treat chapping, etc.; Grigson,
1955) or the leaves being used to curdle milk and
form a buttermilk-like fermented dairy product.
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
Figure 11. Pinguicula moranensis Kunth, cultivated at RBG Kew. Photograph taken by Maarten J. M. Christenhusz.
Today, this is still consumed in the Nordic countries
as filmjölk or tätmjölk (Swedish), tjukkmjølk (Norwegian) or viili (Finnish).
Pinguicula spp. are usually small, rosette-forming
plants. The spurred flowers are produced singly on
stalks from the centre of the leaf rosette and are held
high above the leaves, possibly to prevent carnivory of
potential pollinators. The leaves are usually bright
green or tinged pink or red and are covered in specialized glands. There are two types of glands: stalked
glands producing a slimy secretion that traps insects
(Fig. 11) and sessile glands that produce enzymes.
Insects in search for water are attracted to the droplets produced by the stalked glands. On contact with
an insect, the stalked glands produce more mucus,
entrapping the insect further while it struggles across
the leaf. Some species bend their leaf edges somewhat, bringing additional glands into contact with the
trapped insect. A leaf surface can only trap insects
once, but new leaves are produced that cover the old
ones when these are no longer functional.
There are c. 50–70 species occurring throughout the
temperate Northern Hemisphere, extending south to
the Himalayas, Atlas Mountains and southern South
America. The genus is especially well developed in
the Andes and Central America. An overview of the
genus was provided by Legendre (2002).
Temperate species are well adapted to cold climates
and form winter buds of densely packed noncarnivorous leaves. Roots are poorly developed in
most species and wither in temperate species during
the winter. Epiphytes like P. lignicola Barnhart form
suction cups on their roots to anchor themselves to
mossy branches.
Pinguicula produces a bactericide, preventing
insects from rotting while being digested. The leaves
were known to have a healing power and were used in
European traditional medicine to heal sores and clean
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
wounds. It took until the 19th century for this genus to
be recognized as carnivorous, by Darwin (1875), who
We thus see that numerous insects and other objects are
caught by the viscid leaves; but we have no right to infer from
this fact that the habit is beneficial to the plant, any more
than in the before given case of the Mirabilis, or of the
horse-chestnut [Aesculus hippocastanum]. But it will presently be seen that dead insects and other nitrogenous bodies
excite the glands to increased secretion; and that the secretion
then becomes acid and has the power of digesting animal
substances, such as albumen, fibrin, &c. Moreover, the dissolved nitrogenous matter is absorbed by the glands, as shown
by their limpid contents being aggregated into slowly moving
granular masses of protoplasm. The same results follow when
insects are naturally captured, and as the plant lives in poor
soil and has small roots, there can be no doubt that it profits
by its power of digesting and absorbing matter from the prey
which it habitually captures in such large numbers.
Conversely, the role of bacteria in the digestion
process has been discussed extensively and Lloyd
(1942) concluded:
Pinguicula is a carnivorous plant inasmuch as it catches small
insects and digests them, at least in part, by means of its own
ferments. The possible part played by bacteria is not excluded.
The small genus Genlisea counts c. 20 species in
the tropics of the Americas, sub-Saharan Africa and
Madagascar. They are small terrestrial or aquatic
plants forming a rosette of leaves, and a few single
flowers are held above the rosette that is similar in
shape and colour to those of Pinguicula or Utricularia. The most peculiar feature of this plant is found
underground. There, leaves form a pair of capillary
tubes joined at the tip in a V-shape; there are spiral
grooves down their lengths allowing soil-borne invertebrates and protozoa to enter. Inwardly pointing
hairs prevent the prey from escaping; the only way
they can swim is towards the apex of the tube, where
they are digested (Płachno, Kozieradzka-Kiszkurno &
Świa˛tek, 2007).
It has been suggested that there is a water flow in
these capillary tubes, but this does not seem to be
the case, so an analogy with the digestive tract of
an animal seems misplaced. For example, HeslopHarrison (1976) wrote:
Genlisea, a genus of the same family [as Utricularia] has a
digestive system almost simulating the intestine of an
animal . . . A flow of soil fluid is maintained through the tube
by the secretion of water through the walls of the utricle and
tube. The diet seems mainly to be of protozoa, but small
crustacea and larval forms of other groups are also induced to
enter the tube. Undigested remains accumulate in the utricle.
To simulate an animal digestive system it would be necessary
only to replace the water flow by peristalsis and to provide the
utricle with an anus!
Among angiosperms, Genlisea species have the
smallest known genomes (Greilhuber et al., 2006).
Those of Pinguicula and Utricularia are larger, but
still also fall among the smallest angiosperm genomes.
Martyniaceae are closely related to Pedaliaceae
(sesame, Sesamum indicum L., and relatives) and
have been suggested to be carnivorous (Mameli,
1916). Martyniaceae occur in semi-dry to desert habitats from subtropical North America to tropical South
America, where the peculiarly shaped fruits are distributed by large mammals, the hooves of which get
caught on the hooks of the fruits. Martynia and
Proboscidea are herbs with succulent stems, and the
plants are covered in glandular hairs that produce a
foul-smelling, sticky exudate. Even although the glandular hairs, especially of Proboscidea lutea (Lindl.)
Stapf. (= Martynia lutea Lindl. = Ibicella lutea (Lindl.)
Van Eselt.), catch many insects (Fig. 9F), no uptake of
amino acids has been demonstrated (Rice, 1999;
Wallace, McGhee & Biology Class, 1999). Mameli
(1916) wrote:
Martynia lutea Lindl. is an insectivorous plant. It catches the
insects by means of an abundant viscous substance, having an
acid reaction, secreted by a large number of glandular hairs
with which its above-ground parts are covered and by which
it dissolves albuminous substances by a proteolytic enzyme,
which has the character of trypsin.
Various authors in the 19th century (see Groom, 1897)
suggested that the glands and capitate hairs found in
the lacunae in the scale leaves of some members
of Orobanchaceae, including Lathraea, might be
involved in nutrient absorption and entrapment and
digestion of small organisms. Groom (1897) discounted this, demonstrating that these structures
were instead involved in water excretion. Despite
this, the suggestion that these plants are potentially
carnivorous has persisted in the literature (e.g.
Heslop-Harrison, 1976; Fitter, 1987; Jolivet, 1998).
However, carnivory in Lathraea and its relatives
appears to be mere speculation (see Fay, 2009, for
further details).
Various members of the family have hairs that catch
small insects. Darwin (1875) reported that Nicotiana
tabacum is covered with innumerable hairs of
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
unequal lengths, which catch many minute insects,
but, in his experiments with infusions of meat and
ammonium carbonate, he produced no convincing
evidence of absorption. Zambelli (1929) stated
that ‘Petunia violacea and Petunia nyctaginiflora are
insectivorous plants’ on the basis of experiments demonstrating the presence of proteolytic enzymes, but
was also unable to produce convincing evidence of
absorption. Spomer (1999) demonstrated that leaves
of Solanum tuberosum L. secrete proteinases, but
Petunia hybrida Vilm. does not. Simons (1981) suggested that crop plants and their relatives with sticky
hairs (notably wild tomatoes and potatoes; species of
Solanum L.) are suitable study plants for investigation of ‘degrees of carnivory’.
The Australian trigger plants of the genus Stylidium Lour. are known to trap small insects such as
gnats and midges using mucilage-secreting glandular hairs on their inflorescences and stems. Because
trigger plants are remarkable for their active pollination mechanism, they had not been examined for
carnivory. However, Stylidium uses the same mechanism to trap their pray as Drosera or Byblis, both
genera that occur in similar habitats and often in
the same places where Stylidium is found. Like
Drosera, the glands produce proteases and can thus
digest the insects caught (Darnowski et al., 2006). It
has been shown that amino acids are absorbed by
the surface of Stylidium, so some species of trigger
plants appear to be fully carnivorous (Darnowski,
Moberly & Płachno, 2007). They co-occur with
species of Drosera in many places, so their habitat
preferences fit the syndrome associated with carnivorous plants.
The basal leaves of the common teasel, Dipsacus
fullonum L., are united around the stem, forming a
cup-shaped structure that fills with water after rain.
All sorts of debris and insects get trapped in it, but
no evidence of digestive enzymes or foliar nutrient
absorption has been revealed. Christy (1923) did note
that the fluid collected in the basin formed by the
leaves has a lower surface tension which could be an
adaptation to kill prey.
In some predominantly carnivorous genera such as
Nepenthes and Utricularia a few detritivorous species
are known. Some Malaysian species, such as Nepenthes ampullaria Jack and N. lowii Hook.f., and N.
pervillei Blume from the Seychelles, catch few insects.
Nepenthes ampullaria derives nutrition from fallen
leaf litter, whereas the last two appear to obtain
nutrients from the droppings of birds and tree shrews
that feed on the nectaries in the pitchers and snail
eggs laid on the rim of the pitchers (Corner, 1978;
Clark et al., 2009).
Utricularia purpurea Walter may have partially
lost its appetite for meat. Trapping rates of prey
were significantly lower than in other species of
Utricularia. The eastern purple bladderwort can
still trap and digest prey in its traps, but does so
sparingly. Instead algae, zooplankton and debris are
present in the bladders, suggesting that U. purpurea favours mutualism instead of carnivory (Richards, 2001).
We think that it is evident from the descriptions
above that many plant species have the capacity
to trap and kill insects and other animals and
that some have refined the carnivorous syndrome to
a high degree. Intermediates (the so-called ‘protocarnivorous’ species) clearly do exist, and it is tempting to consider many of these to be good carnivores.
Hartmeyer (1998), referring to species that do not
produce their own digestive enzymes, stated:
The production of enzymes should not be a prerequisite for a
plant to be considered carnivorous – a symbiosis with another
digesting agent should be sufficient. In the past, symbioses
were mistakenly considered strange exceptions, but now it is
apparently a widespread syndrome with carnivorous plants.
Indeed, with some plants it is an integrated part of the
digestive system!
Other species exhibit even less specialized cases, but
they too should not be discounted. The cost–benefit
model for the evolution of carnivory indicates that
there is a trade-off between the costs of carnivory
and benefits to photosynthetic output (and ultimately to enhanced seed production), made possible
by the additional nutrients acquired (Givnish et al.,
1984; Benzing, 1987). The model also implicitly
implies that, in some situations, carnivorous plants
should have advantages over non-carnivorous plants
in the same habitats. In his review of published
data, Ellison (2006) showed that nitrogen, phosphorus and potassium often limit the growth of carnivorous plants, and their use of these elements is
20–50% that of non-carnivorous plants. All data
indicated as well that under no circumstances do
carnivores have a clear-cut advantage over noncarnivorous plants, and thus it appears that car-
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 329–356
nivory is in fact a choice of the lesser of two evils in
difficult circumstances. Carnivores have poor competitive abilities because their lineages became
adapted to living under conditions that were far
from optimal in terms of nutrient availability, and
carnivory represents a slight improvement over
what would otherwise be the case. The habitats in
which carnivores typically occur are those in which
harsh abiotic conditions limit competition between
species, and it is under such abiotic stress that carnivory represents an improved although certainly
not optimal strategy. If the cost–benefit model
cannot be used to explain why vegetable carnivory
has been adopted by species with the full-blown syndrome, then it is difficult to see how it can be
applied in situations where the species are these
intermediate types described above. If mucilagesecreting hairs evolved in response to herbivory
or to attach seeds to animals to aid in their dispersal, their co-option into providing increased
nutrition necessitates minimal additional expense;
it involves absorption of nutrients through roots,
which happens as a matter of course. This minimal
level of carnivory must surely be beneficial and
confer some slight advantage. It is easy to imagine
that this limited response is further constrained by
the phylogenetic legacy inherited from the conditions under which their ancestors evolved and the
limitations imposed by environmental stress in their
current habitats. When confronted with two miserable options, the less miserable wins the day. Fullblown vegetable carnivory obviously threads a
twisting trajectory through the maze of cost and
benefit ‘peaks and valleys’ under highly stressful
environmental conditions, and these are notoriously
difficult to model. The ‘intermediate’ cases described
above are no less difficult to understand, particularly when the basic requirements for being carnivorous, mucilage-secreting hairs, are ubiquitous, at
least in the eudicots to which the majority of carnivores and so-called ‘proto-carnivorous’ (i.e. intermediate) taxa belong. If carnivory is far more
common than previously held because of many
species being subtly carnivorous, then the background comparisons of ‘carnivore vs. non-carnivore’
are also inappropriate because the latter category
includes perhaps many species that are subtly carnivorous through symbioses with other organisms.
The evolution of vegetable carnivores requires a
great deal more study, both in terms of better documentation of the putatively intermediate cases as
well as understanding of its evolutionary context,
which may be constrained as much by phylogenetic
history as by physiological responses. We may be
surrounded by many more murderous plants than
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