Review

Research review
Blackwell Publishing Ltd

Evolving Darwins most wonderful

plant: ecological steps to a snap-trap

Author for correspondence: Thomas C. Gibson1 and Donald M. Waller2

Donald M. Waller 1
205 Danbury Court 2A, DeForest, WI 53532, USA; 2Department of Botany, University of Wisconsin,
Tel: +1 608 263 2042
Email: dmwaller@wisc.edu 430 Lincoln Drive, Madison, WI 53706, USA

Received: 30 March 2009

Accepted: 10 May 2009

Summary

New Phytologist (2009) 183: 575587
doi: 10.1111/j.1469-8137.2009.02935.x
Key words: Aldrovanda, Dionaea, Drosera,
evolution of carnivory, snap-trap, Venus
flytrap.
Among carnivorous plants, Darwin was particularly fascinated by the speed and
sensitivity of snap-traps in Dionaea and Aldrovanda. Recent molecular work confirms
Darwins conjecture that these monotypic taxa are sister to Drosera, meaning that
snap-traps evolved from a flypaper trap. Transitions include tentacles being modified
into trigger hairs and marginal teeth, the loss of sticky tentacles, depressed diges-
tive glands, and rapid leaf movement. Pre-adaptations are known for all these traits
in Drosera yet snap-traps only evolved once. We hypothesize that selection to catch
and retain large insects favored the evolution of elongate leaves and snap-tentacles
in Drosera and snap-traps. Although sticky traps efficiently capture small prey, they
allow larger prey to escape and may lose nutrients. Dionaeas snap-trap efficiently
captures and processes larger prey providing higher, but variable, rewards. We develop
a size-selective model and parametrize it with field data to demonstrate how selection
to capture larger prey strongly favors snap-traps. As prey become larger, they also
become rarer and gain the power to rip leaves, causing returns to larger snap-traps
to plateau. We propose testing these hypotheses with specific field data and Darwin-
like experiments. The complexity of snap-traps, competition with pitfall traps, and their
association with ephemeral habitats all help to explain why this curious adaptation
only evolved once.

I care more for Drosera than the origin of species ... it is a wonderful
plant, or rather a most sagacious animal. I will stick up for Drosera
to the day of my death.
Letter from Charles Darwin to Asa Gray (Jones, 1923)
Introduction
Accounting for the evolution of transitions between forms in
plausible detail represents an important domain of Charles
Darwins theory of natural selection ever since On the origin
of species (Darwin, 1859). Treatises have been written on the
acquisition and loss of eyes, how limbs evolved in quadrupeds,
transitions to terrestrial life, how flight evolved in birds and
bats, the origin of placental mammals, and Darwins abominable
mystery, how angiosperms originated. Many unusual plant
adaptations captured Darwins interest, including the extra-
vagant contrivances by which orchids attract pollinators
(Darwin, 1862), heteromorphic flowers and the wonderful
efficiency of cleistogamy (Darwin, 1877), how plants move
(Darwin, 1880), and various forms of plant carnivory (Darwin,
1875). The remarkably fast responses of Venus flytrap (Dionaea
muscipula Ellis) to insects and simulated prey and their role in

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providing nutrients particularly fascinated Darwin, prompting
him to label it one of the most wonderful plants in the world.
Although Darwin realized that readers might find details about
carnivorous plants dry as dust (letter to R. Cooke at J. Murray,
September 1879) he may have viewed his investigations of
their intricate adaptations as a flank movement on the enemy
as he did his book on orchids (letter to Asa Gray; Darwin,
1862; Sacks, 2008).
With a power Darwin could only have dreamed of, molecular
systematics has allowed us to reconstruct patterns of relation-
ship within and among carnivorous plants. We now know
that plant carnivory evolved at least six times independently,
that pitfall-traps like those of pitcher plants evolved in four
different orders, that sticky flypaper traps evolved in at least
three or four clades and diversified widely within the Droser-
aceae, and that snap-traps of the kind we see in Dionaea and
the waterwheel plant (Aldrovanda vesiculosa L.) evolved once
at least 65 million yr ago somewhere in the Old World (Muller,
1981; Cameron, 2002; Rivadavia et al., 2003). Sundews in
the Droseraceae diversified into at least 175 species in the
former Gondwana and are now particularly diverse in species
and growth forms in Australia (97 species) and South Africa
(18 species). Growth forms range from simple ground rosettes
(15 cm across), to filiform-ensiform leafed rosettes ( 20 cm
tall), to vines (10 cm to 3 m long), to the bush-like Drosera gigantea
(1 m tall). This extreme diversity of forms may reflect displace-
ment as a result of competition for insect resource (Thum,
1986; Gibson, 1991a; Verbeek & Boasson, 1993). The king
sundew, Drosera regia, from South Africa is particularly
noteworthy for having leaves up to 50 cm long and being
closest to the lineage that evolved snap-traps.
Both Dionaea and Aldrovanda were formerly more abundant
and broadly distributed, as known for example from fossil
Palaeoaldrovanda seed fragments from the late Cretaceous
(8575 million yr ago) found in the Czech Republic, the
oldest known remains of a carnivorous plant (Knobloch & Mai,
1984; Degreef, 1997). Although still widespread, Aldrovandas
range is still collapsing, dropping from > 150 to fewer than
36 locations in the last 200 yr as remnant populations suffer
human disturbance and decline (Adamec, 1995). Its world-wide
distribution strongly resembles those found for species in the
unrelated aquatic carnivorous plant genus Utricularia (L.
Adamec, pers. comm.), suggesting parallel adaptations to
capture prey under similar conditions. Dionaea is known only
from wet pine savannas in southeastern North America. Thus,
snap-traps are rare both in the sense of having a single evo-
lutionary origin and in the sense of having a narrow ecological
distribution and shrinking range.
The geographic range of Dionaea has also declined greatly
since its origin more than 60 million yr ago. Land development
and fire suppression continue to eliminate Dionaea populations,
reducing its range to < 10% of its original habitat (300 km2;
Weakley, 2001). Poaching and over-collection for the rare
plant trade continue despite the availability of commercially
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propagated plants (Nickens, 2008). To protect and restore its
habitats to sustain populations of Darwins most wonderful
plant, we advocate listing the species as threatened or endan-
gered under the US Endangered Species Act. Listing would
designate critical habitats, protect against further habitat losses,
strengthen enforcement of anti-poaching laws, and fund further
scientific studies. A surcharge on commercially sold flytraps
could add private resources to acquire, protect, and manage
habitats (Gibson, 2003).
How did snap-traps evolve from sticky-trap ancestors? As
the name implies, snap-traps close suddenly, enclosing their
prey like a mouse- or leg-hold trap, a mechanism clearly distinct
from those found in both sticky traps and Utricularia bladder
traps which suddenly expand to suck in prey. Because the
Venus flytrap appears so different from sundews, it is hard to
imagine how it might have evolved from sundew ancestors
(Williams, 2002). What was the sequence of steps involved in
this transition? What particular ecological conditions and selec-
tive forces favored these steps? Here, we first contrast sticky
traps as found in Drosera with snap-traps as occur uniquely in
Aldrovanda and Dionaea. Although sticky traps and snap-traps
clearly differ greatly in morphology and action, their structures,
physiology, and modes of action share many common features.
Contrary to what some intelligent design proponents have
claimed, these commonalities demonstrate that, although snap-
traps only evolved once, pre-adaptations for all their features
clearly exist in close relatives. We next review the steps involved
in this remarkable transition and introduce the likely selective
forces involved. The most conspicuous such force concerns the
nutrients returned via carnivory. As these vary strongly with prey
size, we construct a model of size-specific carnivory to explore
how evolution could have favored individual features of snap-
traps. This analysis clearly demonstrates how capturing larger
prey brings disproportionate rewards to traps that act swiftly
and strongly enough to retain large prey. We then use field data
to parametrize this model and assess its predictions. Finally,
we outline further studies and data that would allow us to test
these assumptions and predictions in detail. The originality here
lies in going beyond traditional descriptions of trap forms to
explore how such traps function in nature to capture wild prey.
Carnivorous plants also provide model systems for examining
how leaves and other organs diversified into traps to capture
prey (Givnish et al., 1984; Juniper et al., 1989; Ellison et al.,
2003; Barthlott et al., 2007). They have yielded insights into
unique physiological and sensory traits (Williams, 1976;
Adamec, 2000; Volkov et al., 2008; Ellison & Gotelli, 2009),
patterns of phylogenetic radiation (Williams et al., 1994;
Cameron, 2002; Rivadavia et al., 2003), and the importance
of ecological conditions and nutrient limitation (Givnish et al.,
1984; Ellison, 2006; Farnsworth & Ellison, 2008). For further
descriptions of these fascinating plants see Givnish (1989),
Ellison & Gotelli (2001), the books by Rice (2006) and Barthlott
et al. (2007), and websites (e.g. Nickens, 2008; Botanical Society
of America, 2009; Wikipedia, 2009).
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Fig. 1 Related insectivorous plants. The circumboreal sundew, Drosera rotundifolia (a), has three to eight small leaves covered with simple
stalked tentacles that capture insects via a sticky fly-paper trap. Drosera falconeri (b) from northern Australia has stalked glands on the margin
of the leaf blade, sessile glands in the center and prominent blade-like petioles resembling those of Dionaea. Selection to capture larger and
more active prey within Drosera may have also favored elongate leaves to curl around their prey as in Dionaeas closest relative, Drosera regia
(c), and long, rapidly triggered snap-tentacles lacking mucilage as in Drosera pulchella (d). The snap-trap itself evolved once in the ancestor
of both the aquatic plant Aldrovanda vesiculosa (e) and its sister species Dionaea muscipulis (f). Photo credits and permissions from: (a) Juza
(http://www.juzaphoto.com); (b) B. C. Barnes, Florida Carnivorous Plant Society; (c) V. Brown; (d) photographer E. Phlmann and S. and I.
Hartmeyer (http://www.hartmeyer.de/Schnelltentakel_D.htm); (e) L. Adamec; and (f) B. Rice (http://www.sarracenia.com).

stuck on these hairs (Fig. 1b). Further struggles of the prey

Adaptations in sticky traps vs snap-traps
Sticky traps of various forms are evident in all species of the
genus Drosera. Their traps consist of arrays of modified glandular
hairs (modified trichomes, usually termed tentacles) that are
spaced fairly evenly across the leaf surface (Fig. 1a). Small insects,
perhaps attracted to colors, the glandular beads, or scent, become
bring them into contact with more sticky hairs, making escape
more difficult. In addition, Drosera hairs and leaves often
actively bend toward stimulation. Leaf forms vary from small
and round (Drosera rotundifolia), aimed mostly at small ground
prey, to erect elongate leaves (e.g. Drosera regia and Drosera
filiformis) that catch larger, more aerial prey. Larger insects often

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Fig. 2 Escape rates from Drosera filiformis tracyi as a function of
insect size (adapted from Gibson, 1991b).
escape small sticky traps (Fig. 2). As Darwin showed, the
mucilage glands respond to prey by secreting digestive enzymes.
Secretions peak after a few days, and then tentacles and sessile
glands absorb nutrients. Drosera rotundifolia completely digested
a small mass of egg white after 50 h (Darwin, 1875). Selection
may favor rapid digestion and absorption as prey nutrients could
easily wash off. Sundews occupy nutrient-poor environments
and fed plants are more vigorous and set more flowers and
seeds (Darwin, 1875). Both nitrogen (N) and phosphorous
(P) appear important in these habitats.
The impressive snap-traps of Dionaea and Adrovanda act in
a completely different manner (Fig. 1e,f ). They lack sticky hairs,
capturing prey by quickly engulfing them. Dionaea specializes
in catching single prey, an important point. Crawling ground
arthropods may come across traps haphazardly, as argued by
Lichtner & Williams (1977), or they may be attracted to stop
and feed by alluring glands located along the rim of the leaf
(Juniper et al., 1989). These glands secrete UV-reflective sub-
stances that may attract insects or contain poisons (as observed
in some carnivores; Mody et al., 1976). While some insects
may feed and not be caught, prey moving about the margin of
the trap are likely to trigger the trap by touching one or more
of the three trigger hairs projecting from the inner surface of
each trap. If a single hair is touched twice or two separate hairs
are stimulated within 120 s, the trap snaps closed in 0.3 s
(Volkov et al., 2008). Speeds in nature may be even faster as
ground temperatures are hotter and water potential is low.
In Insectivorous Plants and The Power of Movement in Plants
(Darwin, 1880), Darwin and his son Francis emerge as creative
experimentalists, eager to establish which stimuli stimulate
movements, structures, and secretions and curious about how
they transmit information among organs. Darwins customary
attention to detail emerges clearly in his descriptions of the
sticky tentacles of sundews, the glossy curved surfaces of pitcher
plants, and their remarkable secretory glands. The exact mech-
anism of snap-trap closure remained obscure for many years
(Williams & Bennett, 1982; Hodick & Sievers, 1989) but now
appears resolved (Volkov et al., 2008). Darwin hypothesized
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Fig. 3 Relationships between insect size and trap size in Dionaea. The
graph shows the average lengths and estimated biomass for insects
caught on variously sized traps along with their 95% confidence
intervals. Redrawn from Gibson (1991b), fig. 3.
that action potentials were involved as he could paralyze a
tentacle in Drosera by cutting its nerve. He sent flytraps to the
eminent physiologist Sir John Burdon-Sanderson who con-
firmed nerve-like rapid depolarization in Dionaea (Burdon-
Sanderson, 1873; Williams, 1973). Although Darwin faced
opposition and controversy for advancing notions (based on
simple country house experiments) that plants transmit and
respond to stimuli like animals (Morton, 1981; de Chadare-
vian, 1996), we witness here the emergence of experimental
plant physiology.
Teeth along the outer margin of the trap play an important
role (Darwin, 1875, p. 312). After the trap closes, the marginal
teeth interlock to prevent prey escape. Small prey, however,
often escape larger traps (Fig. 3, Darwin, 1875; Jones, 1923).
Darwin conjectured that selection would favor releasing small
prey as the nutrients gained would not repay the costs of diges-
tion. After false alarms or small prey escape, the leaf slowly
opens again, resetting the trap. After the trap closes, it continues
to respond to crawling movements and the presence of protein
by gradually sealing shut along its rim and secreting acidic
digestive enzymes (Williams, 1976; Lichtner & Williams,
1977). This ability to seal reduces prey and nutrient losses and
may allow more complete digestion. Digestion takes 57 d and
we hypothesize that the tight seal allows more complete nutrient
extraction. Well-fed plants photosynthesize at higher rates,
grow faster, flower more, and survive longer (Gibson, 1983).
Strong veins crisscross the lobes in a rip-stop pattern, increasing
its tensile strength and its ability to resist prey escape (T. Gibson,
pers. obs.). Finally, the trap reopens but remains insensitive,
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Table 1. A comparison among characters found in Dionaea, Aldrovanda, and related members of the Droseraceae s.s.*

Other Drosera spp. Drosera regia Aldrovanda Dionaea

Distribution New & Old World; Old World: S. Africa Old World: Disjunct in New World: SE USA
diverse in S. Africa Europe, Africa, SE Asia,
and Australia and Australia
Habit Terrestrial Terrestrial Aquatic Terrestrial
Trapping mechanism Flypaper-trap Flypaper-trap Snap-trap with ~20 trigger Snap-trap with 3 trigger
hairs/leaf lobe hairs/leaf lobe
Glands adaxial glands; adaxial glands; adaxial glands and adaxial glands and abaxial
stalked, vascular stalked, vascular quadrifid glands/hairs; stellate glands; sessile,
sessile, nonvascular nonvascular
Stamens 5 5 5 15
Pollen tetrads Mostly with radial Without radial plates Without radial plates Without radial plates
plates
Grains Multi-aperturate Multi-aperturate Triaperturate Multi-aperturate
Spinose? Yes Yes Yes No
Pollen apertures pores opposite at opposite opposite alternate
tetrad connection
Styles Separate, mostly Separate, undivided Separate, undivided United
divided
Placentation Parietal Parietal Parietal Basal
Seed Small, dust-like Small, dust-like with thin, Large, with smooth, Large, with smooth,
with thin, reticulate reticulate exotesta thickened exotesta and thickened, exotesta
exotesta endotesta
Chromosome # 2n = 20, 30, 32, 40, 2n = 34 (small) 2n = 48 (medium) 2n = 32 (small)
60, 80 (small)

*Note several common traits between Drosera regia and the two snap-trap species. These include the pollen apertures which are operculate,
mostly with channel openings in most other Drosera species whereas Drosera regia, Aldrovanda, and Dionaea all have apertures that are not
operculate and lack channel openings. After Cameron et al. 2002.

allowing the remains to dry and blow away before traps reset
(Barthlott et al., 2007). Traps function two or three times
before becoming defunct.
Traps vary in size and position through the seasons, with
petioles becoming longer and more vertical in summer, then
short and prostrate in winter. Petioles are broader in the spring,
expanding near the trap as a photosynthetic surface. With
shade, petioles become larger and traps become smaller (Roberts
& Oosting, 1958).
Knowing which prey Dionaea captures helps us understand
how traps evolved. Carnivorous plants with traps on the ground
generally capture ground prey, whereas taller traps capture more
flying insects (Gibson, 1983). Dionaea appears specialized for
taking large ground crawling prey (Dean, 1892; Grigg, 1935).
Lichtner & Williams (1977) found 33% ants, 30% spiders,
10% beetles, and 10% grasshoppers with fewer than 5% flying
insects. Recent studies report a similar distribution: 31% spiders,
26% ants and 12% beetles (Hutchens et al., 2007; Hutchens
& Lukens, unpublished). By contrast, sundews usually catch
flying insects although ground traps tend to capture ground
prey (Verbeek & Boasson, 1993).
As Darwin surmised, larger flytraps generally capture larger
prey (Fig. 3, Gibson, 1991b; Hutchens & Lukens, unpublished).
Larger traps also capture prey of a broader range of sizes than
small traps, with occasional very large prey. In summary, the
nectar glands, spaced teeth, rapid closing, crosshatched veins, and
eventual sealing of traps all adapt Dionaea to selectively capture,
retain, and digest larger prey than those caught by most Drosera.
Steps to a snap-trap
The folding of the blade of the leaf itself around the fly is a new fact to
us, and is especially interesting, being a step toward Dionaea
Mrs Treat (1871, p. 463) describing Drosera rotundifolia
Dionaea and its close relative Aldrovanda evolved as monotypic
sister genera from a sundew-like ancestor (Williams et al.,
1994; Cameron, 2002; Rivadavia et al., 2003). These genera
share many traits with each other and with Drosera, including
similar flower and pollen forms (Table 1; see Cameron et al.,
2002 for further discussion). How did snap-traps evolve from
a simple sticky trap? What selected for rapid closure, larger
leaves, and a bigger rosette? Why did this remarkable innovation
only evolve once? The particular transitions included (Barthlott
et al., 2007):
1. modification of responses to prey, including directed move-
ments of tentacles and leaves to increase adhesion and
engulf prey;

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Fig. 4 Scenario for the evolution of snap-traps from Drosera. (a) Basic evolutionary transitions of the leaf as currently understood. (b) Transition
from marginal trichomes in Drosera to marginal teeth in Dionaea. Adapted from Juniper et al. (1989, their fig. 19).
2. acceleration of the rapidity with which prey are detected
and the message is transmitted;
3. evolution of structures to quickly close the trap and engulf
prey;
4. tuning of these responses to only respond to real and suit-
able prey;
5. modification of the structure of marginal tentacles to create
longer and more widely spaced marginal teeth to retain prey;
6. modification of other tentacles to act as trigger sensory hairs;
7. loss of sticky glands from these tentacles and evolution of
recessed digestive glands.
While the exact timing and sequence of these steps remain
uncertain, there can be no doubt that such transitions occurred
in the lineage leading to Aldrovanda and Dionaea. Our goal
here is to explore the ecological forces that acted on a sticky-
trap ancestor to favor these transitions. We are less concerned
with (and qualified to discuss) the remarkable physiological
mechanisms that these traps display. Our inferences are based
on logic, existing structures in related species, a simple model,
and empirical data from contemporary studies. As we lack
fossil intermediate forms, we consider this scenario a series of
hypotheses to test.
Following Mrs Treat, others have made conjectures on how
snap-traps evolved. Williams (1976) carried out fundamental
work on the mechanisms and evolution of sensory physiology
in Droseraceae, including how a flytraps teeth and trigger hairs
lost mucilage in evolving from Drosera tentacles. Snyder (1985)
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outlined how sticky traps in Drosera could have evolved into
a Dionaea trap by tentacles either losing their stalks to become
sessile digestive glands or becoming trigger hairs or marginal
teeth. Givnish (1989) has argued that sticky traps become less
effective in rainy and wet environments, favoring snap-traps.
Degreef (1988) goes further to argue that carnivory began as
an aquatic adaptation to capture detritus in an Aldrovanda-
like ancestor which subsequently evolved into the snap-trap of
terrestrial Dionaea and the sticky traps of Drosera. However,
this appears untenable given recent molecular evidence. Juniper
et al. (1989; see Fig. 4) outlined explicit steps from Drosophyllum
to Dionaea, postulating a loss of tentacles (as in Drosera erythro-
rhiza) with marginal tentacles retained as teeth and trigger
hairs. Eventually, the alluring glands evolved with UV-reflective
secretions.
Several selective forces may have favored snap-traps, including
capturing prey more quickly, capturing larger prey, and selec-
tion to make digestion and nutrient assimilation more efficient
and complete. More rapidly closing traps effectively prevent
escape. Larger prey bring higher rewards. Traps that contain
and process prey more quickly lose fewer nutrients to wind,
water, and microbial decomposition. All these forces were
probably important and interrelate. We focus our discussion
here on selection for larger prey.
Interesting alternatives to snap-traps exist within the Dro-
seraceae. As already noted, tentacles in Drosera are often active,
bending toward stimuli. Leaves also tend to curl around prey
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in response to signals from the tentacles. In Drosera regia
(Fig. 1c) and Drosera capensis, leaves wrap entirely around prey
in as little as 30 min (Juniper et al., 1989). These traits serve
to limit prey escape (and kleptoparasitism) and perhaps aid
digestion. Sensitive tentacles are also an essential pre-adaptation
for (and homolog of ) the trigger hairs in Aldrovanda and
Dionaea. We also see signs of structural divergence and differ-
entiation in several Drosera species (e.g. Drosera binata, Drosera
scorpioides, and Drosera indica) where marginal tentacles are
elongate, extending their reach for insect capture.
Richard Davion discovered another relevant adaptation in
Australian Drosera in the late 1970s as a 9-yr-old. He noted
that the marginal tentacles in Drosera glanduligera lack glue
but respond sensitively to touch by rapidly snapping in to fling
small insects onto the short sticky tentacles there (see video
at http://www.youtube.com/watch?v=zNAqwgPyPX4). The
Hartmeyers (Hartmeyer & Hartmeyer, 2006, 2008) investi-
gated this phenomenon in detail, confirmed Davions discovery,
identified the sensitive area at the tip of the tentacle, and docu-
mented variation in the structure and speed of these snap-
tentacles among several species including Drosera burmanii,
Drosera sessilifolia, Drosera ericksoniae, and Drosera pulchella
(Fig. 1d). The bisymmetric snap-tentacles on D. glanduligera
and D. burmanii are discretely jointed, resembling the hinged
trigger hair in Dionaea. Snap-tentacles on D. glanduligera act
100 times more quickly than those on related species (0.15
vs 515 s). Thus, the morphological diversity, action, speed
and sensory mechanisms of snap-traps are all matched in
Drosera. Furthermore, snap-tentacles seem adapted to capture
ground prey in that six species with ground rosettes in Section
Lamprolepis support snap-tentacles whereas four close relatives
with aerial leaves all lack them (as expected if sticky traps work
better to capture aerial prey; Hartmeyer & Hartmeyer, 2006).
Interestingly, snap-tentacles in D. glanduligera only develop
after three to four leaf generations, suggesting an advantage that
depends on leaf size.
Further transitions include the evolution of glandular ten-
tacles into nonglandular teeth, trigger hairs, and the depressed
digestive glands we see in Dionaea. Interestingly, the glandular
tentacles in several Drosera become shorter on mid-leaves.
Shorter tentacles could provide stronger adhesion, better absorp-
tion, or less breakage from struggling prey. Selection for shorter
and fewer stalked glands would also allow leaves to close more
completely. As tentacles lost their primary role in entangling
prey as closure accelerated, they would be free to diversify in
morphology and function. Costly stalked glandular tentacles
would also be counter-selected, favoring their evolution into
the recessed digestive glands we see in Dionaea (Barthlott
et al., 2007).
The longer leaves we see in some Drosera may thus be adap-
tations to capture not just more prey, but also larger prey. Simple
sticky traps efficiently capture small prey but large prey are
usually stronger, allowing them to escape from, or damage,
sticky traps (Fig. 3; Gibson, 1991b). The higher potential rewards
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Fig. 5 Hypothetical rates of nutrient capture from a sticky trap (as in
Drosera) and from a snap-trap (as in Dionaea) as a function of
arthropod prey size. Sticky traps have the capacity to trap many small
prey efficiently but suffer increasing rates of escape of larger prey,
leading to declines in rates of nutrient capture with increasing insect
size. The higher rewards associated with individual larger prey can
favor mechanisms such as snap-tentacles in Drosera and snap-traps in
Aldrovanda and Dionaea that efficiently capture and retain larger
prey. These returns, however, are less predictable and plateau,
as larger insects are rare.
from capturing larger prey provide strong selection favoring
traps capable of capturing them. Stronger and longer sticky
tentacles and leaves in Drosera can enfold larger prey, but these
move slowly. Snap-tentacles quickly flick small insects into a
sticky trap, but appear less effective at capturing larger insects.
Snap-traps combine speed with the ability to immobilize larger
prey. They could thus bring higher rewards (Fig. 5), particu-
larly if they effectively seal in nutrients.
Modeling the steps
Carnivory exists commonly in species occupying wet, open
habitats where sunlight and water are abundant but nutrients
are scarce (Givnish et al., 1984; Ellison, 2006). Givnish et al.s
(1984) heuristic costbenefit model explains the evolution of
carnivory in such environments. In their model, carnivorys
benefits derive from increased nutrient acquisition, allowing
plants in nutrient-stressed environments to grow more quickly.
To accrue these benefits, carnivorous plants construct costly
traps with specialized structures and physiology with corres-
pondingly diminished capacities for maximizing photosyn-
thesis (Ellison & Gotelli, 2009). The model reasonably and
intuitively assumes that costs increase linearly with increased
investments in carnivory but that benefits plateau beyond a
certain level of investment as traps interfere with one another,
local prey are depleted, and/or additional nutrients are of less
use to the plant. These diminishing returns favor an optimal
level of investment in carnivory that increases in more nutrient-
stressed environments or when prey capture and digestion
become more efficient.
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The Givnish et al. (1984) qualitative model helps to explain

the general circumstances favoring carnivory but makes no
specific predictions regarding the type of trap favored or its
form and selectivity. We therefore extend the model to incor-
porate details regarding two modes of capture (sticky traps vs
snap-traps) and to explore how nutrient returns scale with the
availability of differently sized prey and their escape rates. Like
them, we assume that costs for carnivory increase in propor-
tion to the number and size of traps produced. For sticky traps,
costs also increase in proportion to the number of tentacles
and the investment per tentacle in structures, glands, and
secretions. By contrast, the benefits derived from producing
more traps (or more tentacles and sticky structures) clearly
plateau once they reach a number, size and density sufficient
to capture common prey. More or stickier tentacles and leaves
beyond some optimum would not increase prey capture appre-
ciably as local prey were depleted and these structures came to
compete and interfere with each other, reducing returns per
trap. Selection for more, stronger, and stickier tentacles to cap-
ture larger prey would also be limited as such prey are scarce
and more likely to damage leaves and tentacles. So we expect
Drosera to evolve gracile sticky tentacles dispersed across and
among spreading leaves in an array efficiently designed to cap-
ture many small prey, as observed in Drosera (Fig. 1). Despite
their efficiency at capturing small prey, sticky traps are ineffec-
tive at capturing larger prey with abrupt cut-offs at 1112 mm
in Drosera filiformis tracyi (Fig. 2) and 34 mm in Pinguicula
nevadense (Zamora, 1990). By contrast, Zamoras artificial mimic
trap caught prey of up to 20 mm, demonstrating that larger
Fig. 6 How do rewards from carnivory scale with prey size? This will
prey were available. depend on the spectrum of available prey sizes and their biomass.
For snap-traps, we expect the returns gained via carnivory (a) Empirical abundances of variously sized prey and their associated
to be proportional to prey biomass. That is, we assume that nutrient value (biomass) plotted as a function of prey size (length in
prey have similar nutrient stochiometry and that traps process mm). Curves are fitted from field data derived from 92 insects caught
prey of different sizes and types with similar efficiency. Nutrient at a light trap by T. Gibson at a Holt, Florida bog in July 1975 (omitting
mayflies and dragonflies). Prey length was log normally distributed
levels actually vary among taxonomic groups and arthropods (mean 2.1996; SD 0.9578). The biomass of these potential prey was
of different size, with carnivorous arthropods having more N a power function of length: log biomass (mg) = 1.197 + 2.6463
than herbivores, and %N increasing with body size among log length (mm); r2 = 0.945. (b) Available prey biomass estimated as
carnivores (Fagan et al., 2002). This strengthens the predic- the product of prey abundance and prey biomass (curves shown in a)
tions of our size-selective model. By contrast, %P differs little as a function of prey length. This curve approximates the total
potential return in nutrients available to Drosera and Dionaea in a
with trophic status, declines with size, and is higher in arachnids natural habitat.
among Sonoran arthropods (Woods et al., 2004). However,
these declines in P amount to only 18% over insects ranging
from 50 to 500 mg in size and so we ignore them. We know
of no data on how efficiently traps capture nutrients from associated with that size (Fig. 6b). Interestingly, this prey avail-
differently sized insects or from surface sticky traps vs enclosed ability curve shows a peak at a prey length of c. 20 mm, with
snap-traps. Such results would be of great interest. only a gradual decline beyond. Including the larger prey that
We expect small prey to be far more abundant than larger this sample omitted, or sampling ground arthropods that
prey on general grounds, but data on the size distributions of probably include more large prey, would accentuate returns
potential prey are scarce. The sample in Fig. 6(a) is based on from larger prey. Note that the estimated peak in available
92 insects caught at a light trap near a bog in Florida (T. Gib- biomass occurs at a prey size appreciably larger than those
son, unpublished data). As expected, prey biomass scales as a caught by small Drosera (e.g. D. filiformis tracyi; Fig. 2).
high power of prey length (2.65 in Fig. 6a). We can therefore We hypothesize that selection to capture larger prey favored
estimate the total biomass of potential prey as the product of several traits, including rapid physiological and mechanical
the number of prey available at each size times the biomass responses, elongate marginal tentacles, shorter central tentacles,

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 Research review Review 583

(a) (c)

Prey length (mm) Prey length (mm)

(b) (d)

Prey length (mm) Prey length (mm)

Fig. 7 Estimated rates of prey capture and consequent nutrient return for sticky traps (a, b) and snap-traps (c, d) as functions of prey size. Rates
of capture for sticky traps in (a) are based on the field data for Drosera filliformis traycii reported by Gibson (1991b; the complement of the escape
rates shown in Fig. 2). Rates of capture for snap-traps as envisioned for Dionaea are assumed in graphs (c) and (d) to be normally distributed
around mean prey lengths of 5, 10, and 15 mm with standard deviations equal to the means. Rates of return in (b) and (d) are then taken to
be the product of the measured or assumed capture curves and the biomass of arthropods available at various sizes (see Fig. 6). Note the greater
absolute returns to snap-traps relative to sticky traps as well as the initially sharply increasing returns as a function of trap and prey size.

tentacles lacking glandular secretions, and leaf folding along a
mid-rib. All these traits serve both to retain larger prey within
sticky traps and as pre-adaptations to evolve snap-traps. Larger
insects and spiders tend to also be faster and stronger, reducing
the effectiveness of sticky traps. By contrast, snap-traps are
similarly efficient at capturing prey of all sizes up to a maximum
proportional to their size (Fig. 3). However, the high cost of
building, tripping, and resetting elaborate snap-traps makes
them inefficient for capturing small prey (Fig. 5). As Darwin
conjectured, this would favor mechanisms to allow small prey
to escape, including tuning of the sensitivity of trigger hairs,
spaced marginal teeth proportional to trap size, and only closing
part way initially.
Both prey size and its variation scale with trap size in Dionaea
(Fig. 3). These data allow us to estimate the distribution of
prey sizes for traps of increasing size (Fig. 7c). If we multiply
these curves by the biomass returns associated with these prey
sizes (the data shown in Fig. 6a), we can estimate the nutrient
returns accruing to traps capturing prey of various sizes (Fig. 7d).
This simple model and the data available (which probably
under-sampled larger prey) strongly support the idea that
traps are under selection to capture large prey, particularly for
prey 510 mm in length. Steep increases in biomass as prey
increase in length favor the capture of larger insects, including
exceptionally large but rare prey (the right tails in Fig. 7c).
Snap-traps thus have the opportunity to gain occasional
sweepstakes rewards from large prey that would inevitably
escape sticky traps. Furthermore, traps across a broad range of
sizes face similarly steep increasing returns for taking larger
prey, as shown by the parallel leading edges of the curves in
Fig. 7(d).
Sticky-trap Drosera thus appear to be caught in an evolu-
tionary dilemma. Their traps efficiently capture small prey
(Fig. 7a) with consequent modest returns (Fig. 7b). The steeply
increasing biomass returns from capturing larger prey provide
strong selection to capture larger prey, but such prey are rare,

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unpredictable, and dangerous to them. However, snap-traps slowly (Fig. 6b). The model becomes stronger if potential
have the potential, even at slower speeds, to prevent the escape ground prey include more large insects than this aerial sample.
of larger prey slowed by a sticky-trap and to seal in nutrients Hutchens & Luken (unpublished) recently reported distri-
from large prey that would take longer to digest. Once this butions of prey and trap sizes in Dionaea. They found a roughly
process began, the high returns from larger prey would have normal distribution of trap sizes averaging 1015 mm but
favored mutants with larger, faster, and more efficient traps. ranging up to 30 mm. Prey length correlated with trap length
The nutrients accruing to such plants would allow them to (R2 = 0.24, P < 0.001), as expected, and variously sized traps
grow more quickly and construct larger rosettes with more had similar capture rates (2324%). They interpret the correlation
traps and flowers, important adaptations in their ephemeral as low and note that many traps remained unsprung, leading
fire-dominated habitats. them to conclude that Dionaea does not selectively favor
larger prey. However, a summer drought prevented them from
sampling summer prey, which include large grasshoppers. If
Evidence supporting the model we convert their prey length data to biomass using the empirical
We envision a small sundew ancestor (the size of D. burmanii) equation in Fig. 6, we see that potential prey biomass increases
evolving first into a plant with small traps and then into a strongly with increasing prey size (Fig. 8a). Of course, many
plant able to produce larger traps. The initial transition to snap- traps are empty, but if we smooth these biomass data and
traps may have occurred rapidly, possibly in a small population,
as supported by the high rates of gene substitution seen in
Aldrovanda and Dionaea (Ellison & Gotelli, 2009). This
transition probably occurred in a terrestrial ancestor of Aldro-
vanda and Dionaea able to resist intermittent flooding (as
Dionaea does), with Aldrovanda subsequently evolving its
aquatic habit. We hypothesize that snap-traps evolved to
efficiently capture, immobilize, and digest larger prey. However,
the complex transformations involved in evolving snap-traps,
their particular habitat requirements, and the existence of
alternative means to capture larger insects (including pitfall
pitcher-like traps, elongate sticky traps, and snap tentacles)
together made this a rare event.
We have abundant evidence confirming Darwins conclu-
sion that growth, flowering, and survival in carnivorous plants
all depend strongly on the nutrients provided by captured prey
(Gibson, 1983; Adamec, 1997; Ellison, 2006). Darwin (1875,
p. 301) cites an experiment where a fed plant grew much more
luxuriantly in its growth than others not so treated. Experi-
ments in Aldrovanda (Kaminski, 1987; Adamec, 2000) confirm
that mutants capturing greater insect biomass have higher
fitness. Although additional feeding experiments demonstrating
positive effects exist for Dionaea (e.g. Roberts & Oosting, 1958),
these were not performed in the field. Field studies are critical,
as laboratory feeding experiments rarely replicate native field
soil and light conditions. We should also apply a full set of
treatments (e.g. feeding, starvation, and open to field feeding)
to seedlings lacking reserves and carry out experiments for long
enough to obtain reliable results.
Our model focuses on the size distributions of prey in sun-
Fig. 8 Empirical returns to Dionaea traps from insects of increasing
dews relative to flytraps across traps of various size. We assume size. Data are computed from the lengths of insects caught in Dionaea
that a short terrestrial sundew caught small prey, similar to traps in winter, spring, and autumn of 2006 (Hutchens & Lukens,
other Drosera (Fig. 2). By contrast, Dionaea routinely catches unpublished) using the empirical lengthbiomass relationship shown
larger (1016 mm) prey (Fig. 3). Empirical distributions of in Fig. 6. (a) Linear fit showing the total biomass return from insects
potential prey size and their biomass in a Florida bog (Fig. 6a) caught as a function of insect length, excluding zeros (return
(mg) = 24.873 + 10.271 length (mm); r2 = 0.67). (b) Smoothing
support the notion that biomass returns from arthropod prey spline fit ( = 676) to a smoothed set of the data shown in (a) but
are a steeply increasing function of prey size up to 20 mm in including zeros. Smoothing function is: 0.25 Xi2 + 0.5 X i1 +
length and that potential returns beyond that size decline Xi + 0.5 X i+1 + 0.25 X i+2.

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include zeros (still omitting summer prey), we still see at least
steady returns with increasing prey size (Fig. 8b). These results
reinforce the conclusion that Dionaea traps suffer no reduction
in overall return as prey size increases and gain the potential
to win very high rewards.
A final line of evidence supporting the model comes from
developmental patterns in plant and trap size. Larger Dionaea
plants always produce larger leaves and traps (with ontogeny
perhaps recapitulating phylogeny). However, in almost all other
plants, the number of leaves and other organs increases in pro-
portion to overall plant size, while the size of specific organs
usually increases little or not at all. Instead, in Dionaea, trap
sizes increase markedly as plants grow larger, yet the number
of leaves (= traps) per plant remains steady or even declines.
Hutchens & Luken (unpublished) report 6.77.4 traps per plant
across three classes of increasing trap size. Roberts & Oosting
(1958, p. 202) found mature plants to actually have fewer (4
8) traps than immature plants (1016). Although well-fed
plants can produce more leaves, it is still striking, given general
allometric patterns of growth across the plant kingdom, that
Dionaeas growth pattern would deviate so strongly from that
of Drosera, which always has more leaves when mature. Again,
we find strong evidence that selection has acted strongly to
favor larger traps.
Small traps on small plants appear specialized for capturing
smaller prey, particularly ants, whereas larger traps often catch
spiders and beetles (Hutchens & Lukens, unpublished). Smaller
prey probably provide a steady if modest supply of nutrients of
particular importance for small plants. Dionaea can grow quickly
if nourished, allowing it to construct larger traps to capture
larger prey with much higher nutrient returns. Williams (1980)
found six of 201 traps closing in 24 h in late June, corresponding
to a rate of 0.03 closures per day. At this rate, we expect Dionaea
snap-traps to wait a median time of 23.2 d between meals.
The growing rewards accruing to snap-traps of increasing size
could then support growth, flowering and fruiting, which
would be of particular value in Dionaeas ephemeral habitat.
Needed data and tests
To understand the costs of carnivory, we should seek to quantify
the higher energetic construction and maintenance costs of
different kinds of trap (Ellison & Gotelli, 2009) and how
these scale with trap size. Traps that replace leaves also incur
an opportunity cost of lost photosynthetic capacity. We expect
this to be low in the high-light environments but we should
test this assumption. We might also try to measure how
construction and opportunity costs vary between sunnier and
shadier environments and seasonally. We might also seek to
better understand the role of particular structures and secretions
by estimating their costs. Mutants lacking sticky tentacles or
secretions would be particularly useful here, but genetic variation
for these quantitative traits could also be exploited. How much
energy do the secretory glands along the rim of Dionaea traps
The Authors (2009)
Journal compilation New Phytologist (2009)
Research review Review 585
represent? What do these secretions contain and how effective
are they at attracting and distracting prey? Do they contain
narcotics (cf Mody et al., 1976)? What digestive enzymes are
secreted by the depressed digestive glands, and how does their
quantity respond to the presence of prey of various size? Do
larger insects take longer to digest? Are they digested less
completely?
While prey nutrients clearly enhance the growth of carnivor-
ous plants in nutrient-poor habitats, we should also further
explore these benefits of carnivory. Do the closed traps of
Dionaea allow digestion to proceed more rapidly or more
completely than digestion in the open traps of Drosera? How
are the absorbed nutrients deployed tactically within the plant?
How much do they benefit growth, survival, and reproduction
through the season in plants of various size? Do their benefits
vary with light and nutrient availability? Carefully controlled
field experiments involving feeding, starvation, and ambient
prey treatments across a range of habitats and plant sizes would
be most informative. An ideal experiment might collect data
on the rates of prey capture and escape as a function of both
prey and trap size in various kinds of trap in the same environ-
ment over several seasons to test their relative efficiency varies
under varying conditions, then link these observations to plant
demography to understand how they affect subsequent growth,
survival, and reproduction.
No one has yet tested Darwins conjecture regarding the
value of letting small prey escape. This could be done via simple
experiments involving prey and traps of various size including
treatments to remove the marginal teeth. We should also com-
pare how effective various kinds of trap are in catching prey of
various size. How does the success rate of snap-tentacles depend
on prey and leaf size? How do the mean and variance of prey
size scale with the size of leaves in round vs elongate leaved vs
snap-tentacle sundews? Is Dionaea better adapted to capture
ground-based insects than nearby competing Drosera species?
Are ground prey generally larger than the aerial prey? Also, do
Dionaeas vertical summer traps capture more of these flying
insects?
Our main conjecture here was that snap-traps capture large
prey more efficiently than sticky traps. To test this, we need
additional data on how capture rates and size distributions of
prey vary among sticky traps and snap-traps of varying size.
Such measurements would allow us to calculate the mean and
variance of prey returns for traps of various size directly rather
than depending on the indirect calculations presented. Our
model predicts that prey capture should increase more rapidly
with increasing trap size in snap-traps than sticky traps and that
these returns should extend to larger sizes. How important are
a few large prey in determining a traps total return? What are
the upper limits to capture? Are they set by the capacity of the
trap to engulf prey or by prey strength? What sticky forces
does it take to retain insects of various size? How does insect
strength scale with size? Are the cross veins in flytrap lobes
effective in retaining larger prey?
New Phytologist (2009) 183: 575587
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586 Review Research review
Finally, to infer general evolutionary forces, we should study
additional species and habitats. How do the returns from
carnivory vary across traps of varying size, shape, and orienta-
tion? Do carnivorous plants compete with each other in the
field? How do landscape structure and connectivity interact
with fires and floods to affect meta-population structure and
dynamics in these disturbance-dependent species? Monitoring
patterns of genetic variation within and among populations
would complement such efforts and allow us to assess whether
remaining populations remain knit together via gene flow.
Our understanding of carnivorous plants has significantly
advanced since Darwin carried out his experiments more than
a century ago. We now know far more about their physiology,
morphology, biogeography, and phylogenetic relationships.
Nevertheless, significant gaps remain, particularly in terms of
field data on rates of prey capture and the size specificity of
capture and escape. Such data are vital if we are to understand
the benefits of carnivory and how these favor particular struc-
tures and patterns of allocation. These gaps are all the more
puzzling given the excellent examples we have in Darwins own
work of the power of simple observations and experiments
with carnivorous plants and Zamoras (1990) plea almost
20 yr ago that prey size in relation to adhesion should become
a prime object for study.
Acknowledgements
J. Hutchens and J. Luken kindly shared their paper and data
on prey and trap sizes in advance of publication. S. Williams
educated us in the close similarity of key traits in Drosera and
Dionaea and provided critical references. B. Juniper provided
advice and shared his diagram outlining the scenario in Fig. 4.
K. Elliott patiently drafted figures. E. Althen retrieved books
and references. We thank K. Amatangelo, R. Evans, T. Givnish,
S. Hartmeyer, S. Johnson, S. Williams, and an anonymous
reviewer for providing suggestions on the text. R. Zeimer and
B. Rice discussed rosette sizes in flytraps. L. Adamec, B. Barnes,
V. Brown, S. and I. Hartmeyer, Juza, E. Phlmann, and B. Rice
provided photos for Fig. 1. J.-L. Martin and J.-C. Davidian
provided stimulating and hospitable working environments
for DMW in Montpellier. TCG thanks B. Barry, K. Marsh,
J. Rohan, M. Smith, Gisela, Jane, and others for their support
and dedicates the paper to Ken Marsh.
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The Authors (2009) New Phytologist (2009) 183: 575587

Journal compilation New Phytologist (2009) www.newphytologist.org