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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 Among carnivorous plants, Darwin was particularly fascinated by the speed and
doi: 10.1111/j.1469-8137.2009.02935.x sensitivity of snap-traps in Dionaea and Aldrovanda. Recent molecular work confirms
Darwins conjecture that these monotypic taxa are sister to Drosera, meaning that
Key words: Aldrovanda, Dionaea, Drosera,
snap-traps evolved from a flypaper trap. Transitions include tentacles being modified
evolution of carnivory, snap-trap, Venus into trigger hairs and marginal teeth, the loss of sticky tentacles, depressed diges-
flytrap. 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 acquisition and loss of eyes, how limbs evolved in quadrupeds,
plant, or rather a most sagacious animal. I will stick up for Drosera transitions to terrestrial life, how flight evolved in birds and
to the day of my death. bats, the origin of placental mammals, and Darwins abominable
Letter from Charles Darwin to Asa Gray (Jones, 1923) mystery, how angiosperms originated. Many unusual plant
adaptations captured Darwins interest, including the extra-
vagant contrivances by which orchids attract pollinators
Introduction (Darwin, 1862), heteromorphic flowers and the wonderful
Accounting for the evolution of transitions between forms in efficiency of cleistogamy (Darwin, 1877), how plants move
plausible detail represents an important domain of Charles (Darwin, 1880), and various forms of plant carnivory (Darwin,
Darwins theory of natural selection ever since On the origin 1875). The remarkably fast responses of Venus flytrap (Dionaea
of species (Darwin, 1859). Treatises have been written on the muscipula Ellis) to insects and simulated prey and their role in

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providing nutrients particularly fascinated Darwin, prompting propagated plants (Nickens, 2008). To protect and restore its
him to label it one of the most wonderful plants in the world. habitats to sustain populations of Darwins most wonderful
Although Darwin realized that readers might find details about plant, we advocate listing the species as threatened or endan-
carnivorous plants dry as dust (letter to R. Cooke at J. Murray, gered under the US Endangered Species Act. Listing would
September 1879) he may have viewed his investigations of designate critical habitats, protect against further habitat losses,
their intricate adaptations as a flank movement on the enemy strengthen enforcement of anti-poaching laws, and fund further
as he did his book on orchids (letter to Asa Gray; Darwin, scientific studies. A surcharge on commercially sold flytraps
1862; Sacks, 2008). could add private resources to acquire, protect, and manage
With a power Darwin could only have dreamed of, molecular habitats (Gibson, 2003).
systematics has allowed us to reconstruct patterns of relation- How did snap-traps evolve from sticky-trap ancestors? As
ship within and among carnivorous plants. We now know the name implies, snap-traps close suddenly, enclosing their
that plant carnivory evolved at least six times independently, prey like a mouse- or leg-hold trap, a mechanism clearly distinct
that pitfall-traps like those of pitcher plants evolved in four from those found in both sticky traps and Utricularia bladder
different orders, that sticky flypaper traps evolved in at least traps which suddenly expand to suck in prey. Because the
three or four clades and diversified widely within the Droser- Venus flytrap appears so different from sundews, it is hard to
aceae, and that snap-traps of the kind we see in Dionaea and imagine how it might have evolved from sundew ancestors
the waterwheel plant (Aldrovanda vesiculosa L.) evolved once (Williams, 2002). What was the sequence of steps involved in
at least 65 million yr ago somewhere in the Old World (Muller, this transition? What particular ecological conditions and selec-
1981; Cameron, 2002; Rivadavia et al., 2003). Sundews in tive forces favored these steps? Here, we first contrast sticky
the Droseraceae diversified into at least 175 species in the traps as found in Drosera with snap-traps as occur uniquely in
former Gondwana and are now particularly diverse in species Aldrovanda and Dionaea. Although sticky traps and snap-traps
and growth forms in Australia (97 species) and South Africa clearly differ greatly in morphology and action, their structures,
(18 species). Growth forms range from simple ground rosettes physiology, and modes of action share many common features.
(15 cm across), to filiform-ensiform leafed rosettes ( 20 cm Contrary to what some intelligent design proponents have
tall), to vines (10 cm to 3 m long), to the bush-like Drosera gigantea claimed, these commonalities demonstrate that, although snap-
(1 m tall). This extreme diversity of forms may reflect displace- traps only evolved once, pre-adaptations for all their features
ment as a result of competition for insect resource (Thum, clearly exist in close relatives. We next review the steps involved
1986; Gibson, 1991a; Verbeek & Boasson, 1993). The king in this remarkable transition and introduce the likely selective
sundew, Drosera regia, from South Africa is particularly forces involved. The most conspicuous such force concerns the
noteworthy for having leaves up to 50 cm long and being nutrients returned via carnivory. As these vary strongly with prey
closest to the lineage that evolved snap-traps. size, we construct a model of size-specific carnivory to explore
Both Dionaea and Aldrovanda were formerly more abundant how evolution could have favored individual features of snap-
and broadly distributed, as known for example from fossil traps. This analysis clearly demonstrates how capturing larger
Palaeoaldrovanda seed fragments from the late Cretaceous prey brings disproportionate rewards to traps that act swiftly
(8575 million yr ago) found in the Czech Republic, the and strongly enough to retain large prey. We then use field data
oldest known remains of a carnivorous plant (Knobloch & Mai, to parametrize this model and assess its predictions. Finally,
1984; Degreef, 1997). Although still widespread, Aldrovandas we outline further studies and data that would allow us to test
range is still collapsing, dropping from > 150 to fewer than these assumptions and predictions in detail. The originality here
36 locations in the last 200 yr as remnant populations suffer lies in going beyond traditional descriptions of trap forms to
human disturbance and decline (Adamec, 1995). Its world-wide explore how such traps function in nature to capture wild prey.
distribution strongly resembles those found for species in the Carnivorous plants also provide model systems for examining
unrelated aquatic carnivorous plant genus Utricularia (L. how leaves and other organs diversified into traps to capture
Adamec, pers. comm.), suggesting parallel adaptations to prey (Givnish et al., 1984; Juniper et al., 1989; Ellison et al.,
capture prey under similar conditions. Dionaea is known only 2003; Barthlott et al., 2007). They have yielded insights into
from wet pine savannas in southeastern North America. Thus, unique physiological and sensory traits (Williams, 1976;
snap-traps are rare both in the sense of having a single evo- Adamec, 2000; Volkov et al., 2008; Ellison & Gotelli, 2009),
lutionary origin and in the sense of having a narrow ecological patterns of phylogenetic radiation (Williams et al., 1994;
distribution and shrinking range. Cameron, 2002; Rivadavia et al., 2003), and the importance
The geographic range of Dionaea has also declined greatly of ecological conditions and nutrient limitation (Givnish et al.,
since its origin more than 60 million yr ago. Land development 1984; Ellison, 2006; Farnsworth & Ellison, 2008). For further
and fire suppression continue to eliminate Dionaea populations, descriptions of these fascinating plants see Givnish (1989),
reducing its range to < 10% of its original habitat (300 km2; Ellison & Gotelli (2001), the books by Rice (2006) and Barthlott
Weakley, 2001). Poaching and over-collection for the rare et al. (2007), and websites (e.g. Nickens, 2008; Botanical Society
plant trade continue despite the availability of commercially 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 bring them into contact with more sticky hairs, making escape
Sticky traps of various forms are evident in all species of the more difficult. In addition, Drosera hairs and leaves often
genus Drosera. Their traps consist of arrays of modified glandular actively bend toward stimulation. Leaf forms vary from small
hairs (modified trichomes, usually termed tentacles) that are and round (Drosera rotundifolia), aimed mostly at small ground
spaced fairly evenly across the leaf surface (Fig. 1a). Small insects, prey, to erect elongate leaves (e.g. Drosera regia and Drosera
perhaps attracted to colors, the glandular beads, or scent, become 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 Fig. 3 Relationships between insect size and trap size in Dionaea. The
graph shows the average lengths and estimated biomass for insects
a small mass of egg white after 50 h (Darwin, 1875). Selection caught on variously sized traps along with their 95% confidence
may favor rapid digestion and absorption as prey nutrients could intervals. Redrawn from Gibson (1991b), fig. 3.
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. that action potentials were involved as he could paralyze a
The impressive snap-traps of Dionaea and Adrovanda act in tentacle in Drosera by cutting its nerve. He sent flytraps to the
a completely different manner (Fig. 1e,f ). They lack sticky hairs, eminent physiologist Sir John Burdon-Sanderson who con-
capturing prey by quickly engulfing them. Dionaea specializes firmed nerve-like rapid depolarization in Dionaea (Burdon-
in catching single prey, an important point. Crawling ground Sanderson, 1873; Williams, 1973). Although Darwin faced
arthropods may come across traps haphazardly, as argued by opposition and controversy for advancing notions (based on
Lichtner & Williams (1977), or they may be attracted to stop simple country house experiments) that plants transmit and
and feed by alluring glands located along the rim of the leaf respond to stimuli like animals (Morton, 1981; de Chadare-
(Juniper et al., 1989). These glands secrete UV-reflective sub- vian, 1996), we witness here the emergence of experimental
stances that may attract insects or contain poisons (as observed plant physiology.
in some carnivores; Mody et al., 1976). While some insects Teeth along the outer margin of the trap play an important
may feed and not be caught, prey moving about the margin of role (Darwin, 1875, p. 312). After the trap closes, the marginal
the trap are likely to trigger the trap by touching one or more teeth interlock to prevent prey escape. Small prey, however,
of the three trigger hairs projecting from the inner surface of often escape larger traps (Fig. 3, Darwin, 1875; Jones, 1923).
each trap. If a single hair is touched twice or two separate hairs Darwin conjectured that selection would favor releasing small
are stimulated within 120 s, the trap snaps closed in 0.3 s prey as the nutrients gained would not repay the costs of diges-
(Volkov et al., 2008). Speeds in nature may be even faster as tion. After false alarms or small prey escape, the leaf slowly
ground temperatures are hotter and water potential is low. opens again, resetting the trap. After the trap closes, it continues
In Insectivorous Plants and The Power of Movement in Plants to respond to crawling movements and the presence of protein
(Darwin, 1880), Darwin and his son Francis emerge as creative by gradually sealing shut along its rim and secreting acidic
experimentalists, eager to establish which stimuli stimulate digestive enzymes (Williams, 1976; Lichtner & Williams,
movements, structures, and secretions and curious about how 1977). This ability to seal reduces prey and nutrient losses and
they transmit information among organs. Darwins customary may allow more complete digestion. Digestion takes 57 d and
attention to detail emerges clearly in his descriptions of the we hypothesize that the tight seal allows more complete nutrient
sticky tentacles of sundews, the glossy curved surfaces of pitcher extraction. Well-fed plants photosynthesize at higher rates,
plants, and their remarkable secretory glands. The exact mech- grow faster, flower more, and survive longer (Gibson, 1983).
anism of snap-trap closure remained obscure for many years Strong veins crisscross the lobes in a rip-stop pattern, increasing
(Williams & Bennett, 1982; Hodick & Sievers, 1989) but now its tensile strength and its ability to resist prey escape (T. Gibson,
appears resolved (Volkov et al., 2008). Darwin hypothesized 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 small traps, with occasional very large prey. In summary, the
(Barthlott et al., 2007). Traps function two or three times nectar glands, spaced teeth, rapid closing, crosshatched veins, and
before becoming defunct. eventual sealing of traps all adapt Dionaea to selectively capture,
Traps vary in size and position through the seasons, with retain, and digest larger prey than those caught by most Drosera.
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 Steps to a snap-trap
shade, petioles become larger and traps become smaller (Roberts The folding of the blade of the leaf itself around the fly is a new fact to
& Oosting, 1958). us, and is especially interesting, being a step toward Dionaea
Knowing which prey Dionaea captures helps us understand Mrs Treat (1871, p. 463) describing Drosera rotundifolia
how traps evolved. Carnivorous plants with traps on the ground
generally capture ground prey, whereas taller traps capture more Dionaea and its close relative Aldrovanda evolved as monotypic
flying insects (Gibson, 1983). Dionaea appears specialized for sister genera from a sundew-like ancestor (Williams et al.,
taking large ground crawling prey (Dean, 1892; Grigg, 1935). 1994; Cameron, 2002; Rivadavia et al., 2003). These genera
Lichtner & Williams (1977) found 33% ants, 30% spiders, share many traits with each other and with Drosera, including
10% beetles, and 10% grasshoppers with fewer than 5% flying similar flower and pollen forms (Table 1; see Cameron et al.,
insects. Recent studies report a similar distribution: 31% spiders, 2002 for further discussion). How did snap-traps evolve from
26% ants and 12% beetles (Hutchens et al., 2007; Hutchens a simple sticky trap? What selected for rapid closure, larger
& Lukens, unpublished). By contrast, sundews usually catch leaves, and a bigger rosette? Why did this remarkable innovation
flying insects although ground traps tend to capture ground only evolve once? The particular transitions included (Barthlott
prey (Verbeek & Boasson, 1993). et al., 2007):
As Darwin surmised, larger flytraps generally capture larger 1. modification of responses to prey, including directed move-
prey (Fig. 3, Gibson, 1991b; Hutchens & Lukens, unpublished). ments of tentacles and leaves to increase adhesion and
Larger traps also capture prey of a broader range of sizes than 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 outlined how sticky traps in Drosera could have evolved into
and the message is transmitted; a Dionaea trap by tentacles either losing their stalks to become
3. evolution of structures to quickly close the trap and engulf sessile digestive glands or becoming trigger hairs or marginal
prey; teeth. Givnish (1989) has argued that sticky traps become less
4. tuning of these responses to only respond to real and suit- effective in rainy and wet environments, favoring snap-traps.
able prey; Degreef (1988) goes further to argue that carnivory began as
5. modification of the structure of marginal tentacles to create an aquatic adaptation to capture detritus in an Aldrovanda-
longer and more widely spaced marginal teeth to retain prey; like ancestor which subsequently evolved into the snap-trap of
6. modification of other tentacles to act as trigger sensory hairs; terrestrial Dionaea and the sticky traps of Drosera. However,
7. loss of sticky glands from these tentacles and evolution of this appears untenable given recent molecular evidence. Juniper
recessed digestive glands. et al. (1989; see Fig. 4) outlined explicit steps from Drosophyllum
While the exact timing and sequence of these steps remain to Dionaea, postulating a loss of tentacles (as in Drosera erythro-
uncertain, there can be no doubt that such transitions occurred rhiza) with marginal tentacles retained as teeth and trigger
in the lineage leading to Aldrovanda and Dionaea. Our goal hairs. Eventually, the alluring glands evolved with UV-reflective
here is to explore the ecological forces that acted on a sticky- secretions.
trap ancestor to favor these transitions. We are less concerned Several selective forces may have favored snap-traps, including
with (and qualified to discuss) the remarkable physiological capturing prey more quickly, capturing larger prey, and selec-
mechanisms that these traps display. Our inferences are based tion to make digestion and nutrient assimilation more efficient
on logic, existing structures in related species, a simple model, and complete. More rapidly closing traps effectively prevent
and empirical data from contemporary studies. As we lack escape. Larger prey bring higher rewards. Traps that contain
fossil intermediate forms, we consider this scenario a series of and process prey more quickly lose fewer nutrients to wind,
hypotheses to test. water, and microbial decomposition. All these forces were
Following Mrs Treat, others have made conjectures on how probably important and interrelate. We focus our discussion
snap-traps evolved. Williams (1976) carried out fundamental here on selection for larger prey.
work on the mechanisms and evolution of sensory physiology Interesting alternatives to snap-traps exist within the Dro-
in Droseraceae, including how a flytraps teeth and trigger hairs seraceae. As already noted, tentacles in Drosera are often active,
lost mucilage in evolving from Drosera tentacles. Snyder (1985) 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 Fig. 5 Hypothetical rates of nutrient capture from a sticky trap (as in
small insects onto the short sticky tentacles there (see video 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
at http://www.youtube.com/watch?v=zNAqwgPyPX4). The prey efficiently but suffer increasing rates of escape of larger prey,
Hartmeyers (Hartmeyer & Hartmeyer, 2006, 2008) investi- leading to declines in rates of nutrient capture with increasing insect
gated this phenomenon in detail, confirmed Davions discovery, size. The higher rewards associated with individual larger prey can
identified the sensitive area at the tip of the tentacle, and docu- favor mechanisms such as snap-tentacles in Drosera and snap-traps in
mented variation in the structure and speed of these snap- Aldrovanda and Dionaea that efficiently capture and retain larger
prey. These returns, however, are less predictable and plateau,
tentacles among several species including Drosera burmanii, as larger insects are rare.
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 from capturing larger prey provide strong selection favoring
100 times more quickly than those on related species (0.15 traps capable of capturing them. Stronger and longer sticky
vs 515 s). Thus, the morphological diversity, action, speed tentacles and leaves in Drosera can enfold larger prey, but these
and sensory mechanisms of snap-traps are all matched in move slowly. Snap-tentacles quickly flick small insects into a
Drosera. Furthermore, snap-tentacles seem adapted to capture sticky trap, but appear less effective at capturing larger insects.
ground prey in that six species with ground rosettes in Section Snap-traps combine speed with the ability to immobilize larger
Lamprolepis support snap-tentacles whereas four close relatives prey. They could thus bring higher rewards (Fig. 5), particu-
with aerial leaves all lack them (as expected if sticky traps work larly if they effectively seal in nutrients.
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
Modeling the steps
depends on leaf size. Carnivory exists commonly in species occupying wet, open
Further transitions include the evolution of glandular ten- habitats where sunlight and water are abundant but nutrients
tacles into nonglandular teeth, trigger hairs, and the depressed are scarce (Givnish et al., 1984; Ellison, 2006). Givnish et al.s
digestive glands we see in Dionaea. Interestingly, the glandular (1984) heuristic costbenefit model explains the evolution of
tentacles in several Drosera become shorter on mid-leaves. carnivory in such environments. In their model, carnivorys
Shorter tentacles could provide stronger adhesion, better absorp- benefits derive from increased nutrient acquisition, allowing
tion, or less breakage from struggling prey. Selection for shorter plants in nutrient-stressed environments to grow more quickly.
and fewer stalked glands would also allow leaves to close more To accrue these benefits, carnivorous plants construct costly
completely. As tentacles lost their primary role in entangling traps with specialized structures and physiology with corres-
prey as closure accelerated, they would be free to diversify in pondingly diminished capacities for maximizing photosyn-
morphology and function. Costly stalked glandular tentacles thesis (Ellison & Gotelli, 2009). The model reasonably and
would also be counter-selected, favoring their evolution into intuitively assumes that costs increase linearly with increased
the recessed digestive glands we see in Dionaea (Barthlott investments in carnivory but that benefits plateau beyond a
et al., 2007). certain level of investment as traps interfere with one another,
The longer leaves we see in some Drosera may thus be adap- local prey are depleted, and/or additional nutrients are of less
tations to capture not just more prey, but also larger prey. Simple use to the plant. These diminishing returns favor an optimal
sticky traps efficiently capture small prey but large prey are level of investment in carnivory that increases in more nutrient-
usually stronger, allowing them to escape from, or damage, stressed environments or when prey capture and digestion
sticky traps (Fig. 3; Gibson, 1991b). The higher potential rewards 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 returns accruing to traps capturing prey of various sizes (Fig. 7d).
mid-rib. All these traits serve both to retain larger prey within This simple model and the data available (which probably
sticky traps and as pre-adaptations to evolve snap-traps. Larger under-sampled larger prey) strongly support the idea that
insects and spiders tend to also be faster and stronger, reducing traps are under selection to capture large prey, particularly for
the effectiveness of sticky traps. By contrast, snap-traps are prey 510 mm in length. Steep increases in biomass as prey
similarly efficient at capturing prey of all sizes up to a maximum increase in length favor the capture of larger insects, including
proportional to their size (Fig. 3). However, the high cost of exceptionally large but rare prey (the right tails in Fig. 7c).
building, tripping, and resetting elaborate snap-traps makes Snap-traps thus have the opportunity to gain occasional
them inefficient for capturing small prey (Fig. 5). As Darwin sweepstakes rewards from large prey that would inevitably
conjectured, this would favor mechanisms to allow small prey escape sticky traps. Furthermore, traps across a broad range of
to escape, including tuning of the sensitivity of trigger hairs, sizes face similarly steep increasing returns for taking larger
spaced marginal teeth proportional to trap size, and only closing prey, as shown by the parallel leading edges of the curves in
part way initially. Fig. 7(d).
Both prey size and its variation scale with trap size in Dionaea Sticky-trap Drosera thus appear to be caught in an evolu-
(Fig. 3). These data allow us to estimate the distribution of tionary dilemma. Their traps efficiently capture small prey
prey sizes for traps of increasing size (Fig. 7c). If we multiply (Fig. 7a) with consequent modest returns (Fig. 7b). The steeply
these curves by the biomass returns associated with these prey increasing biomass returns from capturing larger prey provide
sizes (the data shown in Fig. 6a), we can estimate the nutrient strong selection to capture larger prey, but such prey are rare,

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584 Review Research review

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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Research review Review 585

include zeros (still omitting summer prey), we still see at least represent? What do these secretions contain and how effective
steady returns with increasing prey size (Fig. 8b). These results are they at attracting and distracting prey? Do they contain
reinforce the conclusion that Dionaea traps suffer no reduction narcotics (cf Mody et al., 1976)? What digestive enzymes are
in overall return as prey size increases and gain the potential secreted by the depressed digestive glands, and how does their
to win very high rewards. quantity respond to the presence of prey of various size? Do
A final line of evidence supporting the model comes from larger insects take longer to digest? Are they digested less
developmental patterns in plant and trap size. Larger Dionaea completely?
plants always produce larger leaves and traps (with ontogeny While prey nutrients clearly enhance the growth of carnivor-
perhaps recapitulating phylogeny). However, in almost all other ous plants in nutrient-poor habitats, we should also further
plants, the number of leaves and other organs increases in pro- explore these benefits of carnivory. Do the closed traps of
portion to overall plant size, while the size of specific organs Dionaea allow digestion to proceed more rapidly or more
usually increases little or not at all. Instead, in Dionaea, trap completely than digestion in the open traps of Drosera? How
sizes increase markedly as plants grow larger, yet the number are the absorbed nutrients deployed tactically within the plant?
of leaves (= traps) per plant remains steady or even declines. How much do they benefit growth, survival, and reproduction
Hutchens & Luken (unpublished) report 6.77.4 traps per plant through the season in plants of various size? Do their benefits
across three classes of increasing trap size. Roberts & Oosting vary with light and nutrient availability? Carefully controlled
(1958, p. 202) found mature plants to actually have fewer (4 field experiments involving feeding, starvation, and ambient
8) traps than immature plants (1016). Although well-fed prey treatments across a range of habitats and plant sizes would
plants can produce more leaves, it is still striking, given general be most informative. An ideal experiment might collect data
allometric patterns of growth across the plant kingdom, that on the rates of prey capture and escape as a function of both
Dionaeas growth pattern would deviate so strongly from that prey and trap size in various kinds of trap in the same environ-
of Drosera, which always has more leaves when mature. Again, ment over several seasons to test their relative efficiency varies
we find strong evidence that selection has acted strongly to under varying conditions, then link these observations to plant
favor larger traps. demography to understand how they affect subsequent growth,
Small traps on small plants appear specialized for capturing survival, and reproduction.
smaller prey, particularly ants, whereas larger traps often catch No one has yet tested Darwins conjecture regarding the
spiders and beetles (Hutchens & Lukens, unpublished). Smaller value of letting small prey escape. This could be done via simple
prey probably provide a steady if modest supply of nutrients of experiments involving prey and traps of various size including
particular importance for small plants. Dionaea can grow quickly treatments to remove the marginal teeth. We should also com-
if nourished, allowing it to construct larger traps to capture pare how effective various kinds of trap are in catching prey of
larger prey with much higher nutrient returns. Williams (1980) various size. How does the success rate of snap-tentacles depend
found six of 201 traps closing in 24 h in late June, corresponding on prey and leaf size? How do the mean and variance of prey
to a rate of 0.03 closures per day. At this rate, we expect Dionaea size scale with the size of leaves in round vs elongate leaved vs
snap-traps to wait a median time of 23.2 d between meals. snap-tentacle sundews? Is Dionaea better adapted to capture
The growing rewards accruing to snap-traps of increasing size ground-based insects than nearby competing Drosera species?
could then support growth, flowering and fruiting, which Are ground prey generally larger than the aerial prey? Also, do
would be of particular value in Dionaeas ephemeral habitat. Dionaeas vertical summer traps capture more of these flying
insects?
Our main conjecture here was that snap-traps capture large
Needed data and tests prey more efficiently than sticky traps. To test this, we need
To understand the costs of carnivory, we should seek to quantify additional data on how capture rates and size distributions of
the higher energetic construction and maintenance costs of prey vary among sticky traps and snap-traps of varying size.
different kinds of trap (Ellison & Gotelli, 2009) and how Such measurements would allow us to calculate the mean and
these scale with trap size. Traps that replace leaves also incur variance of prey returns for traps of various size directly rather
an opportunity cost of lost photosynthetic capacity. We expect than depending on the indirect calculations presented. Our
this to be low in the high-light environments but we should model predicts that prey capture should increase more rapidly
test this assumption. We might also try to measure how with increasing trap size in snap-traps than sticky traps and that
construction and opportunity costs vary between sunnier and these returns should extend to larger sizes. How important are
shadier environments and seasonally. We might also seek to a few large prey in determining a traps total return? What are
better understand the role of particular structures and secretions the upper limits to capture? Are they set by the capacity of the
by estimating their costs. Mutants lacking sticky tentacles or trap to engulf prey or by prey strength? What sticky forces
secretions would be particularly useful here, but genetic variation does it take to retain insects of various size? How does insect
for these quantitative traits could also be exploited. How much strength scale with size? Are the cross veins in flytrap lobes
energy do the secretory glands along the rim of Dionaea traps effective in retaining larger prey?

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Finally, to infer general evolutionary forces, we should study Botanical Society of America. 2009. Carnivorous plants/insectivorous plants.
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