CarnivorousPlantsandTheirPrey,

Pollinators,andPeculiarPartners

PaulD.Johnson

UndertheadvisementofDr.DavidInouye
July15,2005
What then distinguishes the carnivorous plants from the rest of the

plant world? Why should we still share the feelings of the

naturalists of

the 18th Century who regarded them as miracula naturae?

Francis Ernest Lloyd (1)

Table of Contents

The Plants

Introduction......4

Numbers and General Distribution of the Carnivorous Plants.5

Carnivorous Plants Defined?6

Abiotic Conditions of Carnivorous Plant Habitats...9

Benefits and Costs of Carnivory to Plants..11

The Prey

Carnivorous Trap Designs..16

Pitfall Traps.16

Sticky Flypaper Traps.19

Spring Traps20

Lobster-pot and Combination Traps...21

Prey Items...22

The Pollinators

Pollination...27

Temporal Separation of Flowers and Traps27

Spatial Separation of Flowers and Traps....29

Other Means of Isolating Pollinators and Prey.......30

2
Carnivorous Plant Floral Design.....32

Insect Pollinators.33

Self-compatibility and Vegetative Reproduction in Carnivorous Plants35

The Peculiar Partners

Other Partnerships...36

General Features of Inquiline Communities...38

Bacterial Symbionts40

Insect Symbionts.37

The Sarracenia-Wyeomyia System.43

Darlingtonia-Inquiline Symbioses..45

The Nepenthes bicalcarata-Camponotus Ant Symbiosis...46

Roridula-Pameridea Interactions....48

Other Carnivorous Plant Symbioses...49

Robbers, Cheaters, and Other Crooks.50

Final Thoughts

Future Thoughts..52

Strange World ....54

3
Desperate for a drink, the famous naturalist Alfred Wallace

drank the liquid from a group of pitcher plants while exploring

Malaysia. Although the fluid was full of dead insects and

looked uninviting, he wrote in 1890 that he and his friends

found it very palatable, though rather warm, and we all quenched

our thirst from these natural jugs. They must have been almost

delirious with dehydration to have quaffed a few pitchers, as one

local name for these plants translates to the place where rats

pee.

Simon D. Pollard (2)

THE PLANTS

Introduction

Predation. It conjures up those images of a big, toothy animal stalking another and

bloodily disposing of its victim, such as the classic version of Tyranosaurus rex assaulting a

Triceratops. A female lion (Panthera leo) with jaws locked around the throat of an African

buffalo (Synceros caffer) while others from her pride latch onto the preys back. The great white

shark (Carcharodon carcharias) rocketing from beneath into its second-favorite victim seal-

shaped surfers (Homo sapiens subspecies californiadudeus). Many organisms in nature actively

4
capture prey; many others passively wait for the prey to come to them. The animal kingdom is

filled with examples of stationary or immobile predators. Alligator snapping turtles

(Macroclemys temminckii), for example, hunt by lying in wait on the bottom of rivers and lakes.

Their mouths are held open and a worm-like lure in the mouth attracts unsuspecting prey (3).

Trap-door spiders of the family Ctenizidae build underground tunnels and wait below the

burrows lid until prey is within easy reach (4). Goose barnacles (Lepas anatifera) are sessile

invertebrates that extend feathery leg-like appendages to capture small fish and cnidarians (5).

And countless other examples of ambush predators could be listed from Kingdom Animalia.

Some fungi, about 150 species, are sessile and predatory (6). Species such as Arthrobotrys

dactyloides and A. oligosperma produce ring-shaped hyphae that ensnare microscopic nematodes.

These fungi also apparently attract nematodes with pheromones and use toxins to immobilize

their prey (7, 8). Predatory fungi, protists, bacteria, and especially animals do not seem to be

contrary to our understanding of predator-prey relationships (3, 5, 7, 9).

Plants, however, are commonly thought of as the nice guys of the natural world,

passively serving as fodder for any number of other organisms. At their worst, plants may

produce noxious toxins or painful structural defenses to protect themselves while still remaining

at the mercy of herbivores an erroneous but common view. Plants that have the ability to seek

out animal prey are conundrums and are usually seen as turning the tables on animals (1, 10).

Yet, such plants the carnivorous plants can be found scattered across the plant kingdom and

the planet. These plants are generally very well-equipped to attract and incapacitate their victims

and so quietly go about the business of successful predation (1, 11).

Numbers and General Distribution of the Carnivorous Plants

Francis Ernest Lloyds watershed work The Carnivorous Plants (1942) identified about

450 species of carnivorous plants (1). In the more than fifty years since that time, another 150

have been added and more may follow (12, 13, 14). The approximately 600 currently identified

species of carnivorous plants come from seventeen genera in about ten families of angiosperms

5
and may be either monocots or dicots (12, 13, 15, 16). With about 220 species in the genus, the

bladderworts (Utricularia spp.) are the most numerous of the carnivorous species accounting for

about one-third of all species (12). Carnivorous plants occur in a variety of forms from the

shrubby Roridula dentata to the lengthy vines of Nepenthes mirabilis, from the bear traps of

Aldrovanda vesiculosa to the pitfall tanks of the bromeliad Brocchinia reducta, from the

aquatic Utricularia inflata to the Venus flytrap (Dionea muscipula), the worlds most famous

plant (1, 10, 12, 13, 15, 17). These plants populate every continent, aside from Antarctica, but

have several centers of distribution around the world (10). North America has the most known

carnivorous species with the southeastern United States showing a particularly diverse

assemblage characterized by several species of Sarracenia pitcher plants (10, 12, 14). Central

and South America are second behind their northern neighbor in species richness with

Heliamphora and Pinguicula being especially important genera (10, 12). Next in order of

diversity comes Australia with Byblis and the ubiquitous genera Drosera with Utricularia

providing many of the species, too (1, 10, 12). Southeast Asia and South Africa are also

important centers of carnivorous plant diversity characterized by Nepenthes and Roridula,

respectively (12). Other important genera of carnivorous plants include Aldrovanda, Cephalotus,

Drosophyllum, Genlisea, and Triphyophyllum (15, 18, 19).

Carnivorous Plants Defined?

Some species like those of the genera Roridula and Byblis have variously fallen from and

been returned to the ranks of carnivorous plants causing the number of carnivorous species to

fluctuate over time (13, 14, 17). This has partly been the result of an inconsistent definition of

carnivorous plants during the last century-and-a-half of study (12, 15). As inquiry into

carnivorous plants has progressed, a working distinction has been established to identify those

species; however, some debate remains (12, 13, 14). Givnish et al. (1984) helped somewhat to

standardize the definition of carnivorous plants by proposing that these plants are characterized

by adaptations that allow active attraction and capture of prey and subsequent digestion and

6
absorption of prey tissues near the plant surface (10, 12, 15, 18). These characteristics of

botanical carnivory could be provided through either morphological, physiological, or

behavioral features (20). The Givnish et al. (15) definition of carnivorous plants also required

that the plants gain some degree of ecological fitness (e.g., greater chances of survival, greater

degrees of pollen production, or larger numbers of seeds produced) from the process of carnivory.

While many plants perform one or more of Givnish et al.s four functions, carnivorous

plants do each of these (10, 12, 15, 18). To illustrate the differences between a true carnivorous

plant and a non-carnivorous one, consider some of the countless plants that meet some of these

requirements. The non-wind-pollinated angiosperms, for instance, use a variety of mechanisms

such as bright colors, nectar rewards, and ultraviolet light patterns to attract organisms such as

bugs, bats, or birds for the purpose of pollination (10, 14, 21). Some insect-pollinated plants may

even briefly detain their pollinators in order to increase the likelihood of pollen transfer (14).

This would provide a large number of flowering plants with two of the four characteristics used to

define carnivorous plants. South American bucket orchids (Coryanthes spp.), for example,

generate pools of fluid in the cup-shaped flower; these pools trap pollinators. To escape their

disconcerting bath, the insects must crawl out of the pool by a route that passes the anthers and

stigmas, thus allowing pollination (21, 22). Even capturing and killing insects may not indicate

carnivory. Unicorn plants (Proboscidea spp.) have sticky leaves that trap insects which

subsequently die on the plant (14). Plants in this genus, however, apparently do not absorb

nutrients from the victims (1, 14). Similarly, the absorption of nutrients directly from organic

sources does not necessarily signify carnivory. Absorption of nutrients directly from organic

matter by a plant that does not possess attractant, digestive, and trap structures would characterize

that plant as a saprophyte instead of a carnivory (15). Even the infamous Audrey II in the 1986

version of Little Shop of Horrors, would not qualify as a true (were she real) carnivorous plant

because she did not attract her own prey but instead relied on Seymour Krelborn to feed her

7
human flesh no less (14, 23). Carnivorous plants do not eat humans unless one is to believe

very suspect 19th Century stories from Madagascar or the Philippines (1, 14, 24).

The accepted definition of carnivorous plants has not always ended the sometimes

contentious inclusion or exclusion of a plant from the carnivorous category (12, 17, 18). Some

genera (or species) generally considered to be carnivorous have been periodically or permanently

de-classified and vice versa because the plants lacked one or more of the required characteristics

(12, 14, 15). The South African genus Roridula has been categorized as both carnivorous and

non-carnivorous (10, 12, 14). Some authorities omit it from the ranks of carnivorous plants

because, although Roridula captures insects with the sticky hairs found across its surfaces, the

genus does not have structures designed to digest the killed insects (10, 17, 18). Consideration of

Byblis species of Australia as a carnivorous plants has varied over time. Byblis have sticky traps

to capture insects but they lack structures to attract their prey and apparently do not produce

digestive enzymes (15, 17). Other debatable genera of carnivorous plants include Proboscidea,

Myartynia, Catopsis, Craniolaria, Ibicella, and the bromeliad Brocchinia. These, too, are

sometimes disqualified because of the lack of evidence for production of enzymes that

breakdown trapped prey (18). Conversely, cobra lilies or California pitcher plants (Darlingtonia

californica), sun pitchers (Heliamphora spp.), and some North America Sarracenia pitcher plants

lack digestive enzymes but are usually considered true carnivorous plants (8, 12, 17, 20, 25).

As research into these species progresses, some suggest that the definition of carnivorous

plants should be broadened to include digestive symbioses between the plants and their obligate

or facultative inhabitants (17, 20, 26). Anderson and Midgley (20) propose that carnivorous

plants need not possess their own digestive structures or enzymes as long as they have host-

specific, obligate symbionts that serve the same function. Some carnivorous plants including

Roridula, Byblis, and Drosera may gain a nutritional advantage indirectly from the actions of

associated invertebrate symbionts (17, 20). Roridula, for example, apparently gains some

advantage from prey capture but requires the breakdown of its trapped quarry by hemipterans in

8
order to obtain the nutrients (20). Likewise, Hartmeyer (17) identified several species of plants

that had arthropod symbioses that aid in the breakdown and subsequent absorption of nutrients

from captured prey. Among the species included were plants in the genera Drosera, Nepenthes,

Sarracenia, and Darlingtonia, all of which have been traditionally considered carnivorous even

though they lack digestive enzymes (15, 17). Other carnivorous plants appear to rely on bacteria

and other organisms to break down prey before nutrient absorption can occur (10, 15). The

Givnish et al. (15) description of carnivorous plants allowed that some species conventionally

identified as carnivorous should continue to be viewed as such on logical or historical grounds.

They still considered bladderworts (Biovularia, Polypompholyx, Utricularia) and butterworts

(Pinguicula) as carnivorous even though some or all of the species in these genera apparently

lack prey attractants or digestive ability. If alternative pathways such as digestive mutualists

are accepted as a feature that meets the Givnish et al. parameter of some unequivocal

adaptationwhose primary result isdigestion of prey, then more species may be deemed

carnivorous and a new level of ecological study (and wonder) may be opened or expanded (15,

20, 26).

Abiotic Conditions of Carnivorous Plant Habitats

While the definition of carnivorous plants may be a bit difficult to generalize, the habitat

in which these plants are found is relatively consistent. Carnivorous plants tend to be found in

ecosystems that are low in nutrients, high in moisture, and high in sunlight (10, 13, 15). The

paucity of soil nutrients in these sites is offset by the availability of high numbers of insects or

other potential prey items (12, 27). Supplementing low soil nutrients with prey capture thereby

allows carnivorous species to out-compete species without such nutritional supplements (12, 28).

Examples of ecosystems that meet most or all of these specifications include bogs, wet pine

savannas, marshes, swamps, and fens (12, 13, 15). Some carnivorous species extend into less

characteristic habitats such as shady epiphytic perches, dry deserts, limestone cliffs, serpentine

soils, and standing freshwater. Again, these habitats are generally low in nutrients but may be

9
shady, aquatic, or arid abiotic conditions not generally thought to be ideal for carnivorous plant

success (12, 15, 18, 29). When carnivorous plants flourish in such atypical habitats, the

environments are often seasonally wet or sunny, which may open a temporal window of

advantage for carnivory (12, 15). Pinguicula vallisneriifolia and Drosophyllum lusitanicum are

representative of carnivorous species that are quite successful in predominately dry

Mediterranean locales (15, 28). Some Nepenthes species provide other examples of carnivorous

plants found in non-carnivorous habitats. Nearly 10% of Nepenthes species are epiphytes found

beneath dense shade. Carnivory among epiphytes is especially low, however, due to poor light

intensities beneath host tree canopies (15). Oddly enough, some bladderworts (Utricularia spp.)

live within tanks of epiphytic bromeliads (1). Carnivorous plants, in general, tend to perform

more poorly under low light (30).

Acidic soil seems to be another prerequisite for the occurrence of carnivorous plants. A

good indicator of favorable carnivorous plant habitat, in fact, is the occurrence of Sphagnum

moss, a species indicative of acidic soils (12, 31). Sphagnum moss increases soil acidity as it

slowly decomposes; this acid-generating decay, in turn, further limits nutrient availability and

thereby favors carnivorous plants (8, 12, 31). Essential plant nutrients may be tied up or simply

lacking in the soil and, therefore, unavailable for plant absorption (8). Securing limited nutrients

by way of carnivory allows carnivorous plants a much needed mechanism to increase the uptake

of nitrogen and other elements. The carnivorous plants gain a competitive advantage over nearby

plants unable to supplement their poor nutrition with mineral-rich insects (11, 12, 14).

Fire-dominated ecosystems can prove favorable to some carnivorous plant species as

well. Much of the current work on fire and carnivorous plants has been done in North America

with pitcher plants. Sarracenia alata in the southeastern United States, for example, thrives in

wet pine savannas that incur fires approximately every three years (13). The endangered

Alabama canebrake pitcher plant (S. rubra ssp. alabamensis), similarly, is much more successful

when annual or biannual fires burn its bog habitat. Without such a fire regime, secondary

10
succession leads to woody plant growth that shades out the carnivorous species (32). Such

ecosystems have the low nutrient availability coupled with high light intensity and moisture that

provide most carnivorous plants a competitive advantage against non-carnivorous plants (10, 13).

A study of Sarracenia alata and S. psittacina also found comparable results. After controlled

burns, these species produced more foliage in the absence of competition from woody invaders

for sunlight. Flower production, however, decreased a year after fire in both burned and

unburned treatments. The authors of the study suggested that regularly occurring fires may be

necessary for these carnivorous plants to obtain reproductive maturity and success (33). Fire

suppression stifles seed recruit and seedling establishment in species like Sarracenia alata (33,

34). Some carnivorous plant species may require fire to overcome a seeds dormancy or to

increase its exposure to sunlight (33). Low litter abundance, indicative of an established fire

regime, favors carnivorous plants, too (13). When litter was removed from sites with Drosera

capillaris, seedling densities increased (35). The removal of litter through events such as fire

apparently allows some carnivorous plants to increase the likelihood of colonization, germination,

and seedling survival. More light and exposed soil provides a better nursery environment for

seeds and young plants (33, 35). Additionally, fires destroy carnivorous plant pests that may

otherwise overwinter in or on the plants (11).

Carnivorous plants rarely produce persistent seedbanks and vegetative propagation

appears to play a major role in their reproduction (13, 14, 31). In temperate regions, seeds that do

remain for several years in the soil seedbank may require an extended period of dormancy before

germination occurs (36). Within a relatively few years, increases in woody competitors or the

accumulation of vegetative litter could significantly reduce the success of fire-dependent

carnivorous plants. In only six years, for example, fire suppression could cause Sarracenia alata

and S. psittacina plants to lose more than 95% of their foliage biomass. Combine such a decline

in vegetative parts with poor seedling establishment and fire-dependent carnivorous could be in

serious trouble (33, 34).

11
 While low nutrients, scarce litter, high light, and low pH allow carnivorous plants a

competitive advantage and influence their geographic occurrance, temperature does not appear to

be a major factor in carnivorous plant distribution. Carnivorous plants can be found from the

taiga to the equator and south to the high latitudes of South America (12, 37). Only high-salinity

aquatic ecosystems appear to be entirely off-limits to carnivorous plants. Brackish and marine

environments are probably too nutrient rich to allow carnivorous plants a competitive advantage

over their more non-carnivorous neighbors (12, 14).

Benefits and Costs of Carnivory to Plants

Carnivory provides a means for plants to augment mineral uptake in nutrient-poor

environments thereby allowing carnivorous plants to compete successfully in such sites (10, 12,

25, 38). The degree to which carnivory benefits the plant, however, varies (13, 15, 28, 39).

Generally, as the trapping mechanism becomes more costly to build or maintain, the amount of

nitrogen derived from prey capture tends to increase. Some Drosera species with energy-

expensive, motile leaf traps, for example, may derive nearly 90% of their nitrogen from insect

prey. Pitcher plants such as some Heliamphora as well as Darlingtonia californica build very

large pitfall traps and obtain more than 75% of their nitrogen budget from trapped prey (13). See

Table 1 for a partial list of the percentage of nitrogen derived from insects in various carnivorous

species. Abiotic factors also influence the total benefit carnivory affords a plant (28, 30, 40, 41).

Benefits from carnivory can be enormous. Based on his study of Drosera in Florida, Gibson (42)

predicted insect capture could increase the biomass of the carnivorous plant up to two hundred

times that of starved plants.

Table 1 Relative contribution of insect nitrogen content to total nitrogen content for
carnivorous plants. In Ellison and Gotelli (13).
Mean %
Trap type Growth habit Species insect
nitrogen
Bladder Aquatic Utricularia vulgaris 51.8
Bladder Terrestrial Polypompholyx multifida 21.0

12
 Sticky leaf Rosette Drosera rotundifolia 26.5
Sticky leaf Rosette Drosera erythrorhiza 19.6
Sticky leaf Vine Drosera macrantha 54.2
Sticky leaf Vine Drosera modesta 34.5
Sticky leaf Vine Drosera pallida 87.1
Sticky leaf Vine Drosera subhirtella 35.6
Sticky leaf Erect, low growing Drosera huegelli 57.3
Sticky leaf Erect, low growing Drosera menziesii 36.7
Sticky leaf Erect, low growing Drosera stolonifera 51.4
Sticky leaf Erect, tall Drosera gigantean 49.1
Sticky leaf Erect, tall Drosera heterophylla 47.2
Sticky leaf Erect, tall Drosera marchantii 64.7
Pitfall Rosette Cephalotus follicularis 26.1
Pitfall Vine Nepenthes mirabilis 61.5
Pitfall Rosette Darlingtonia californica 76.4
Pitfall Rosette Heliamphora sp. 79.3
Pitfall Rosette Brocchinia reducta 59.8
Pitfall Rosette Sarracenia purpurea 10.0

Historically, nitrogen acquisition was, and usually still is, seen as the most important

benefit of carnivory in plants (38, 43). Proteins from prey items provide a supplemental nitrogen

source for the carnivorous plant and amino acids may be absorbed directly by trichomes within

the traps (15, 43). Some recent work suggests that carnivory may be of greater importance with

respect to phosphorus uptake (10). Whether nitrogen or phosphorus, carnivory provides a

mechanism by which this group of plants can acquire the most limited soil nutrient in the

environment via prey digestion. Our understanding of the benefits of carnivory seems to be

expanding, too. Investigations into Sarracenia flava have indicated greater absorption of not only

phosphorus but also sulfur and several required ions from prey (25, 38). Again, carnivory

appears to provide an avenue to nutrients not readily available in the soil but easily accessible

from organic prey (12). The poorly developed root systems found in many carnivorous genera

apparently compound the problem of acquisition of soil nutrients (13, 31). Sarracenia purpurea,

just one example among many, increases absorption of ammonia nitrogen from insects trapped in

pitchers to offset low nitrogen uptake through the relatively small root system (38).

13
 Digestion of prey provides carnivorous plants with several distinct advantages in their

growth, maintenance, and reproduction (28). Carnivorous plants with insect prey show greater

rates of photosynthesis (25). Improved photosynthesis, however, may be a secondary result of

carnivory. In studies of carnivorous plants in which supplemental prey was provided, nitrogen

acquisition from insects, although relatively small, resulted in a much larger uptake of soil

nitrogen (13). Prey capture may, therefore, indirectly increase carbon fixation (13, 15). More

nitrogen equates to either more shoot production or an improved photosynthetic rate (15).

Carnivory may not necessarily result in a total gain with respect to photosynthesis. The need to

produce traps may lead to production of fewer photosynthetic leaves or leaves that have lower

rates of photosynthesis (13). A tradeoff accordingly exists between maintaining photosynthetic

leaves versus carnivorous traps (13, 15, 39, 40). When soil nitrogen is readily available, for

example, plants may opt for production of more photosynthetic leaves and fewer traps (39). To

illustrate, Sarracenia purpurea invests more into construction of photosynthetic leaves than traps

when nitrogen is non-limiting. In some cases, these pitcher plants may entirely neglect the

production of traps. Greater investment in leaf tissue when nutrients are not limiting is especially

important to carnivorous plants because their photosynthetic rate may be as much as half of that

of non-carnivorous neighbors (13). The transition from predominately leaf to trap or trap to leaf

production can occur relatively quickly (39). Selective investment into traps or leaves becomes

especially important for plants that occur in ecosystems that diverge from the carnivorous norm

of high light, high moisture, and low nutrients (13).

As shade increases or moisture decreases, carnivory becomes less beneficial. Shaded

plants are typically more limited by light than soil nutrients; therefore, carnivory becomes an

expensive burden that could take resources away from construction of more photosynthetic tissue

(28, 30, 39). Trap production and its associated features such as digestive enzymes and nectar or

other lures become too costly to produce because of the lowered rates of photosynthesis (13, 15,

40). Low light environments, too, may necessitate initiation of more photosynthetic surface at the

14
expense of carnivorous traps. A study with Drosera rotundifolia, for example, found a

significant increase in leaf production when plants were grown under shaded conditions.

Concurrently, a reduction in the investment to carnivory was seen; trap leaves were less sticky

than those growing in high-light, low-nutrient conditions (40).

A similar situation occurs in drier sites; low moisture availability limits photosynthesis

and negates the usefulness of carnivory (15). Moist, sunny sites usually will be nitrogen or

phosphorus limited since carbon is readily available; therefore, carnivory becomes most

advantageous in nutrient poor, high light environments (15, 38, 39). Nutrients provided to the

plant by carnivory become less important in more fertile soils because aboveground parts could

be better utilized to capture light instead of prey. As soil nutrients increase, carnivorous plant

growth fails to increase significantly with insect-derived minerals (15).

While carnivory clearly supplements nutrient uptake in high light, low nutrient

environments, benefits from the process may be seasonal in some instances, or depend on the age

of the plant (13, 15, 39, 40). The sticky flypaper traps of Triphyophyllum, for instance, are

produced just prior to the beginning of the rainy season as insect availability dramatically

increases (15). Seasonal heterophylly dictates that carnivorous plants concentrate resources to

photosynthetic structures during certain times of the year when soil nutrients are readily available

but light or water is low (8). The degree of carnivory may differ with the age of plants, too.

Several groups of carnivorous plants including the Cephalotus, Darlingtonia, Nepenthes, and

Sarracenia must obtain sufficient nitrogen from the soil when young because their pitchers are

immature and non-functioning. As plants age, their pitchers operationally mature and the bulk of

nitrogen acquisition is obtained from carnivory (12, 13). Aquatic carnivorous plants may also

rely more heavily on traps as they age. The bladderwort Utricularia vulgaris, for instance,

depends entirely on nitrogen from the water column until bladders are well-developed.

Organisms captured in bladders then provide about half of the plants nitrogen budget (13).

15
 Regardless of the connection between carnivory, photosynthesis, plant age, and other

factors, carnivorous plants gain a reproductive advantage through greater nutrient uptake from

their prey (13, 41, 44, 45). Abundant prey consumption, when other resources are available,

leads to greater potential investment into reproductive structures and nectar (10, 25, 28, 40).

Following flowering, seed production is also enhanced. Carnivorous plants with prey-derived

nutrients produce more seeds and those seeds have higher nutrient content (15). As with other

aspects of carnivory though, a compilation of environmental conditions can confound attempts to

pinpoint exact relationships between prey capture and reproduction (39, 41, 46). For instance,

Drosera growing under low light may be forced to invest less energy into bloom production.

Plants found in shady sites may also allot less energy into insect-trapping mucilage. Poor trap

quality then leads to less prey capture and, consequently, less nutrient availability. With fewer

nutrients to sink into reproductive structures, flowering would be diminished. Low light, then,

can influence flowering directly and/or indirectly (30, 40, 41).

THE PREY

Carnivorous Trap Designs

Carnivorous plants, like all organisms in nature, interact with a wide assortment of other

organisms in a variety of different capacities. The most noticeable and best studied interactions

of these plants involve the predator-prey encounters of carnivory. Carnivorous plants act, in

effect, like lay-in-wait predators: attracting, capturing, and consuming invertebrate prey. Small

vertebrates are apparently taken by carnivorous plants occasionally, too, but these victims may be

accidental and provide little, if any, nutritive benefit to the plant (10, 12, 14). Even other plants

may provide fodder; in these cases, traps may be designed to capture a veritable, vegetative,

detrital rain (12, 25). And with approximately six hundred species of carnivorous plants, the

methods of prey capture might be suspected to be diverse. They are. Five different methods of

16
prey capture are generally recognized including pitfall traps, sticky flypaper traps, spring traps,

lobsterpot traps, and a combination of more than one trap type (1, 11, 12, 15, 24).

Pitfall Traps

The simplest and probably the most geographically widespread method of prey capture

involves the use of pitfall traps such as those found in several genera of pitcher plants (11, 12,

13). Plants in four different families use this method including dicots of the Nepenthaceae,

Sarraceniaceae, and Cephalotaceae and monocots in the Bromeliaceae (13, 15). Pitcher plants are

nearly ubiquitous. The Nepenthaceae has species scattered across the planet and is represented

by the Nepenthes, a genus focalized in southeast Asia. Genera from the Sarraceniaceae include

the North American pitcher plants Sarracenia and Darlingtonia and South American sun pitchers

Heliamphora. The Australian Cephalotus typify plants with pitfall traps from the Cephalotaceae

(12). If bromeliads (Bromeliaceae) like Brocchinia reducta and Catopsis berteroniana are

accepted as truly carnivorous, then their water-filled tanks would qualify as pitfall traps (15, 16,

24). As further evidence to support inclusion of Brocchinia reducta as a carnivorous plant, this

bromeliad possesses a tank fluid that smells like sweet nectar, similar to the South American

pitcher plant Heliamphora heterodoxa, which probably lures insects to its trap (15).

The basic design of a pitfall trap includes a leaf modified into a pitcher or cup, a trap

coating to aid prey in their descent into the pitcher, liquid to detain and drown the hapless

victim, and a means to digest the prey (1, 12, 25, 43, 47). Generally, pitchers consist of several

distinct regions within the traps that provide the means to achieve carnivory (25). In the North

America Sarracenia pitcher plants, for example, potential prey first encounter the attractive

zone upon entry into the pitcher. Prey-luring mechanisms in the attractive zones may consist of

enticing scents, nectar rewards, colorful trap designs, or ultraviolet light patterns (1, 10, 14, 25,

48). Pitfall traps may mimic floral structures as a means to attract misguided pollinators (11, 12).

Some pitchers have patterns of more transparent tissue interspersed between thicker layers of

17
tissue. This gives the pitcher an open, lighted appearance which, once inside, confuses insect

visitors and causes them to move towards the digestive fluid thinking it the route to escape (12).

Pitchers may be very straightforward in their construction simply consisting of vegetative

cups filled with fluid. Most pitchers, however, are modified to hinder the escape of insects and

thereby increase the efficiency of prey capture (12, 27, 49). A lip or ledge may protrude inward

from the top edge of the pitcher requiring insects to attempt an upside-down walk in order to free

themselves from the trap. This often results in the prey falling down into the fluid-filled pitcher

(11, 12). Some Sarracenia have hoods over the pitchers to inhibit prey from flying out as well as

prevent rainfall from filling the pitfall trap (10). Nepenthes albomarginata, an Indonesian pitcher

plant, has a unique lure to entice termite prey. These plants have trichomes around the rim of the

pitchers that attract scouting Hospitalitermes bicolor termites. Scouts, in turn, signal their cohorts

to feed on the living plant tissue. The termites feed on the hairs and gradually move into the

pitcher in search of more of the apparently tasty trichomes. Once inside the pitcher, the termites

slip into the fluid-filled traps en masse and are ultimately digested by the plant. The attractive

zone may also be covered with downward pointing hairs that prevent exit and guide insects

towards the digestive fluid (25, 50). Within about one hour of the start of termite activity, the

insects succeed in completely grazing away the rim hairs, which ends the feeding. Pitchers are,

by this time, filled with termites (51).

Below the attractive zone in many pitfall traps lies a second zone often lined with

nectaries to attract insects further into the pitcher (1, 25). The second zone as well as the third are

typically covered with slippery secretions that cause prey to lose their grasp on the trap walls and

plummet into the digestive zone below (1, 12, 25, 50). Aldehyde-based wax crystals secreted by

the plant cover these zones and may either break away as insects move about or prove to be too

slick for prey to gain a foothold (25, 43, 47). An insects weight and its appendage design helps

determine what insects get caught, too. As an example, larger insects without adhesive pads on

their legs may easily slip from the waxy pitcher surface (50).

18
 The eminent end to the pitfall pathway is the fourth zone the site of digestion and

absorption. Lower portions of pitchers are filled with a veritable chemical concoction that may

be a mixture of rainwater, plant fluids, digestive enzymes, and often a plethora of symbionts (14,

25, 29, 38). Plant-derived fluids may be comprised of digestive enzymes to break down prey,

wetting agents to ensure thorough coating of prey items with the digestive enzymes, and sedatives

to limit struggling and possible escape by the victims (12, 14). Many plants with pitfall traps

including Cephalotus and Nepenthes species and some Sarracenia (S. flava, for example) produce

their own digestive secretions (15). Others, however, appear to require digestive mutualists to

complete the carnivorous process. Plants such as Heliamphora, Darlingtonia, and Sarracenia

purpurea apparently fail to produce digestive enzymes and, instead, depend on invertebrate and

bacterial pitcher occupants to break apart prey and dissolve the bodies of trapped victims (12, 15,

25, 52). For some species like Sarracenia purpurea however, secretion of plant-derived digestive

enzymes remains equivocal (25, 38).

Sticky Flypaper Traps

A second common means of prey capture is the use of sticky flypaper traps. These traps

are found in five different dicot families including Byblidaceae, Dinocophyllaceae, Droseraceae,

Lentibulariaceae, and Roridullaceae (13). The Byblidaceae has two carnivorous species from the

genus Byblis while Dinocophyllaceae includes one species, Triphyophyllum peltatum (12, 13, 15).

Two species of Roridula were previously placed in the Byblidaceae but are now included in the

Roridullaceae (16). The Droseraceae includes about 90 to 100 species of Drosera sundews as

well as the Portuguese sundew Drosophyllum lusitanicum (15, 53). Carnivorous species from the

Lentibulariaceae include about 35 butterworts in the genus Pinguicula (15).

Regardless of the family, carnivorous plants with flypaper traps generally have glandular

leaves that secrete a sticky, mucus-like substance. These secretions may appear to be nectar to

unsuspecting insects (1, 11, 12, 15). The leaves often give off an enticing odor that smells either

floral or fungal. Various species have their own unique odor designed to attract specific prey

19
(12). When an insect or other invertebrate lands on the trap, it becomes ensnared in a quagmire

of mucus. As the animal struggles to free itself, it becomes even more coated in the mucus which

leads to complete incapacitation and eventual suffocation (1, 12). Drosera sundews illustrate the

method of prey capture and consumption in sticky flypaper traps with an added twist. Sundews

have their leaves modified into tentacle-like structures covered with mucus-laden hairs. The hairs

are tipped with an attractive droplet of nectar that draws insects in (10, 54). Movement of prey

insects along the hairs initiates electrical impulses along the tentacles and triggers surrounding

hairs to fold in on the struggling victim (16, 54). The curled tentacles provide additional contact

points for digestive glands to break down the prey (12). Digestive enzymes produced by the plant

begin the process of tissue degradation at the site of prey capture (12, 54). In genera like

Pinguicula, leaves do not coil around the victim; instead, the prey is simply immobilized in the

mucus (12).

Spring Traps

While pitfall and sticky flypaper traps are quite widespread across genera, the most

common type of trap is the spring-trap design (15). This is due to the large number of

bladderworts (Utricularia spp.) the greatest number of species of carnivorous plants with such

trapping mechanisms. The spring-trap carnivorous plants are housed in two families, the

Droseraceae and Lentibulariaceae. The monospecific Dionea and Aldrovanda are placed in the

Droseraceae while the Lentibulariaceae contains about 280 species of Utricularia, one species of

Biovularia, and two species of Polypompholyx (1, 15, 53). Biovularia species are sometimes

included in the genus Utricularia (55).

Spring-traps differ from genus to genus and include a variety of forms as diverse as the

bear trap design of the Venus flytrap (Dionea muscipula) or the waterwheel plant (Aldrovanda

vesiculosa) and the suction traps of the aquatic Utricularia species (12, 15). The variance in trap

construction launches a disparity in trap nomenclature. For example, spring-traps are sometimes

referred to as active steel-traps with Dionaea and Aldrovanda or mousetraps in the Biovularia,

20
Utricularia, and Polypompholyx (1). As just mentioned, the aquatic, bladder-like traps on the

underwater leaves of bladderworts (Utricularia spp.) are often referred to as suction traps (10, 12,

55).

While the details of spring-traps vary, the overall mechanism is generally the same prey

items set off a triggering mechanism that causes the trap to react very rapidly to entomb the

victim (1, 12, 16). Venus flytraps, for instance, use a hinged bear-trap design to capture larger

insects. Leaves close as insects move about the surface and hair-like extensions along the leaf

margins interlock to contain insect prey (12). To elicit a response, insects must stimulate trigger

hairs on the trap surface. As potential prey moves across trigger hairs on the trap, electrical

impulses in the hairs initiate an enzyme-mediated pumping of hydrogen ions into cells along the

outer edges of the trap. Leaf traps very speedily snap closed as the cell walls expand with the

acid influx (54). Prey insects must, however, rapidly vibrate trap hairs two or more times before

the leaves respond and close (12). As a captured insect flails about in an attempt to escape, it

continues to stimulate the trigger hairs causing the traps to intensify their grasp (12, 56). Ants in

traps, for example, may continue to struggle for up to eight hours during which time the traps

continue to compress their prey. Captured prey eventually succumb to highly acidic leaf

secretions (56). The need to stimulate trigger hairs repeatedly also provides a mechanism for the

plants to ignore insignificant prey items or abiotic stimuli such as rainfall (12, 56, 57). If

entrapped insects are not above a certain size-threshold, they fail to continue the necessary

excitation of trigger hairs. Small insects can crawl out of the closed trap to freedom. Without

stimulation, the traps open again by the next day (12, 56). If prey is captured, digestion requires

about a week. Then, the trap opens again to await the next meal (12).

Aquatic bladderwort traps function similarly to snare prey. Suction, or bladder traps, are

inflated and when triggered by prey such as Daphnia generate a vacuum that sucks the victim

inward (10, 12, 16). Prey items come into contact with long hairs originating from a door

covering the bladder. Stimulation of the hairs initiates the pumping of ions from the inner portion

21
of the trap. An osmotic reaction occurs as water follows the movement of the ions (16, 24).

Osmotic changes in the bladder force the door open thereby creating a vacuum that sucks the prey

inward much like the action of a predatory fish as it gulps in a smaller fish (16, 58).

Lobster-pot and Combination Traps

Less common trap types occur in several dozen species of carnivorous plants. About

thirty-five species of West African and eastern South American Genlisea in the family

Lentibulariaceae use a lobster pot trap to capture prey passively (1, 12, 15). Lobster pot traps

allow insect prey to enter but the design is such that they are confounded in their attempts to find

an exit (1, 12). In the Genlisea, aquatic protozoan prey are allowed to move into the trap but

inward pointing hairs inhibit the organism from retracing its path. In hope of reclaiming its

freedom, the prey keep moving towards the digestive zone of the plant (16).

Several species of carnivorous plants use a combination of trap types. The parrot pitcher

plant (Sarracenia psittacina) of the southeastern United States normally captures prey in pitfall

traps. When its bog or pond edge habitats flood, however, inundated S. psittacina pitchers act as

lobster pot-traps to take aquatic prey (1, 12). The tropical pitcher plant Nepenthes inermis,

similarly, uses pitfall traps but also includes a sticky flypaper-like covering on its interior walls

(12). See Table 2 for a breakdown of carnivorous genera and their mode of prey attraction,

capture, and digestion.

Table 2 Presence (+) or absences (-) of adaptations for active prey attraction, capture, and
digestion in genera of carnivorous plants. In Givnish et al. (15).
Genera (no. sp.) Prey attraction Prey capture Prey digestion Trap type
Brocchinia (1) + passive - pitfall
Heliamphora (6) + passive - pitfall
Darlingtonia (1) + passive - pitfall
Sarracenia (9) + passive +/- pitfall
Cephalotus (1) + passive + pitfall
Nepenthes (71) + passive + pitfall
Genlisea (35) - passive + lobsterpot
Drosera (90) - + + flypaper
Drosophyllum (1) + + + flypaper
Byblis (2) - + + flypaper

22
Pinguicula (35) - + + flypaper
Triphyophyllum (1) - + + flypaper
Dionaea (1) + + + spring-trap
Aldrovanda (1) - + + spring-trap
Utricularia (280) -/+ + + spring-trap
Biovularia (1) - + + spring-trap
Polypompholyx (2) - + + spring-trap

Prey Items

The type of prey taken by carnivorous plants varies from species to species. Some

carnivorous species are generalists while others specialize on a very limited diet or even just one

prey species. Carnivorous plants, in general, consume a wide variety of prey items, from protists

to insects to vertebrates, and some may even be partially herbivorous (2, 10, 12, 13, 14, 15).

Insects appear to be the most common type of prey across the carnivorous plant world. In

Roridula, Anderson and Midgley (20) discovered insect prey represented by nineteen different

species in four orders. The bromeliad Brocchinia reducta was found to have thirty-one families

of insect prey from six orders (15). Similarly, the North American pitcher plant Sarracenia

purpurea contained prey from twenty-nine families of insects and six orders. (8). Cresswell (49),

in a study of S. purpurea, identified insects from thirteen orders and forty-nine families trapped

within pitchers. The major orders represented by the aforementioned examples include

Coleoptera, Collembola, Diptera, Hemiptera, Homoptera, Hymenoptera, Lepidoptera, and

Orthoptera (8, 15, 20).

Insects are not the only types of prey taken by carnivorous plants. Aquatic carnivorous

plants like Aldrovanda and Utricularia may feed on the larvae of insects like mosquitoes but they

also consume daphnia, rotifers, and even small, immature fish (14). The genus Genlisea may

have a diet that lacks insects entirely as there is evidence these carnivorous plants specialize on

protozoans (12, 14). Other invertebrate prey items recovered from carnivorous plants include

annelids, centipedes, millipedes, crustaceans, slugs, snails, mites, spiders, and even slime molds

23
(10, 12, 14). Nematodes could also serve as nourishment for some carnivorous plants.

Agamomermis nematodes, more than 15 cm long, were isolated from Sarracenia purpurea;

however, this species is a parasite of grasshoppers. When the grasshoppers are captured, their

parasitic passengers may inadvertently become prey as well (8). Vertebrates are occasionally

recovered from larger pitchers of some temperate and tropical carnivorous species (8, 14). Small

frogs and lizards have been found in large pitchers of Sarracenia purpurea (8). Tropical

Nepenthes species sometimes capture amphibians as well as small rodents and birds. If the

animal is too small to extract itself from a large, deep pitcher, it would drown and apparently be

digested by its captor (14). Vertebrates, however, are probably rare prey items and those that do

get caught in pitchers may be sick or dying (12, 14). Small amphibians or reptiles that feed on

insects attracted to the carnivorous plants may at times accidentally slip into pitfall traps they are

robbing and then themselves become the meal (8, 14).

Some carnivorous plants may supplement their diets with either plant or animal waste

(12, 20, 59). Nepenthes ampullaria produces a plethora of pitchers along the forest floor using

their pitchers to trap plant material falling from trees overhead (12, 14). Some Pinguicula and

Drosera species may also gain nutrients from pollen grains, seeds, spores, and leaves that settle

onto the sticky-leaf traps (59). Other carnivorous plants obtain essential nutrients from excrement

left behind by animal visitors (12, 20, 26). In one example, sunbirds (Nectariniidae) defecate into

the pitchers of Nepenthes lowii as they feed on plant exudates (12). Several genera of

carnivorous plants including Roridula, Sarracenia, and Darlingtonia may rely similarly on

inquiline mutualists. Anderson and Midgley (20, 26), for instance, found that Roridula dentata

may gain approximately three-fourths of its nitrogen budget from the feces of Pameridea species,

hemipterans that feed on insects captured by the carnivorous plant.

Because of trap design, attractants, or prey characteristics, many carnivorous species

capture a disproportionate number of a specific type of prey, sometimes specializing on a single

assemblage of organisms (10, 12, 13, 51, 60). Pitfall traps tend to capture large, flying insects

24
such as butterflies, moths, flies, and wasps as well as foraging insects such as beetles and ants

(14, 60). The sticky flypaper traps of genera like Drosera, Byblis, and Pinguicula collect mostly

smaller flying insects such as flies, gnats, and moths (12, 14, 60). Venus flytraps generally

capture crawling or poor-flying insects (14, 56). In classic studies of Venus flytraps, 40% of the

prey found in traps were entirely flightless while more than a third (37%) were clumsy fliers

(56). The apparent size selection of insect prey is often the result of the potential victims ability

to extract itself from the traps (12, 56, 60). With Venus flytraps, for instance, smaller insects may

not trigger trap closure because they do not stimulate enough trap hairs. If traps do close, these

insects can crawl out of the trap. By preventing capture or allowing escape of smaller insects, the

Venus flytrap eliminates prey that may be more expensive to capture and digest than nutritionally

beneficial (12, 60). Insects above a certain size threshold, however, not only trigger trap closure

but encourage trap tightening as they struggle to free themselves (56). Similarly, Gibson (60)

showed Drosera filiformis and Pinguicula lutea species with sticky flypaper traps capture

many insects across several size classes. Larger insects, however, invariably were able to escape

within thirty minutes of capture, the time required for digestion to begin. Large, crawling insects,

in general, seem to be better equipped to escape from sticky flypaper traps than smaller insects

(60). Other large insects such as bumblebees (Bombus spp.), for example, may chew their way

through the walls of pitchers when they become stuck in pitfall traps (10). Many carnivorous

plants, therefore, apparently have an optimal size of prey (27, 60). Others, like pitfall trap species

such as Sarracenia leucophylla, catch a variety of prey sizes (60).

Not only does the type of prey vary from group to group, but the efficiency of trapping

also differs among species and even between traps of an individual plant (27, 49, 60, 61).

Cresswell (49), for example, found half of Sarracenia purpurea pitchers studied did not catch any

prey over the course of nearly two months. Larger S. purpurea pitchers tend to capture a

disproportionally large biomass of prey compared to smaller pitchers. Pitchers with greater

nectar production and pigment variation also tend to collect more prey (61). At least with respect

25
to S. purpurea pitchers, only a small percentage of traps account for the majority of successful

captures. Only about half of S. purpurea pitchers studied in a Michigan bog caught any prey; of

those that did, less than 10% of traps brought in two-thirds of prey biomass (49). Even efficient

traps may have low insect-capture rates. Using video cameras to record insect visits, Newell and

Nastase (27) found S. purpurea captured less than 1% of insects entering pitchers. In contrast,

Fish and Hall (62) observed one S. purpurea pitcher trapping forty houseflies over the course of

forty-eight hours.

Lures and attractants are important features of differential prey selection. The tropical

pitcher plant Nepenthes rafflesiana, for example, produces a fragrant attractant that entices

mainly flying pollinators such as bees, moths, and thrips. Its cousin N. gracillis appears to be less

fragrant and captures more crawling insects such as beetles and some true bugs (13). Some

carnivorous plants even produce patterns that appear to mimic flowers; these also tend to attract

insect pollinators (12). As with many flowers, carnivorous plants may use trap-generated nectar

to encourage visitation by potential prey (10, 12). Sarracenia flava, for example, attract bees and

other nectar eaters by exuding a sweet reward (10). Such nectaries are often placed above

pitfall traps. As the foraging nectivore tires or slips, it falls into the trap (12, 14).

Lures and/or traps may also be modified to attract differing prey as the growing season

progresses (15). Sarracenia flava appears to capture mostly bees early in the year and wasps

later. Some pitcher plants also apparently produce typical pitfall traps in the spring but, in the

fall, traps look like flowers and catch moths almost to the complete preclusion of other prey items

(10). Triphyophyllum peltatum produces a greater number of sticky flypaper traps just before the

rainy season and its associated explosion of potential insect prey (15). Darlingtonia californica

have traps as young plants but as the plant ages, the pitcher location, as well as prey selection,

changes. Young pitchers do not stand upright but, instead, lay on the ground. The tongue-like

portion of the trap apparently attracts ground-dwelling insects until the pitcher is capable of

26
standing erect. Mature pitchers of D. californica are then positioned to capture flying insects

(29).

Some carnivorous species, especially many of the temperate and tropical pitcher plants,

generally consume a wide variety of prey; their only preference seems to be careless insects (38).

Other species specialize in a narrow range of prey types. Ants seem to be a favorite food of

several carnivorous plants and various designs seem to increase the likelihood of myrmecophagy

(10, 12, 15, 51). Givnish et al. (15) found eight genera of ants representing about 90% of prey in

the carnivorous bromeliad Brocchinia reducta. The ants appeared to be attracted to nectaries on

the plant (15). In North America, Sarracenia minor and S. psittacina appear to consume only

ants (10, 11). Sarracenia minor may possess a specialized ant attractant or the ants, which prefer

slightly arid soils, may simply be more available in the drier habitats in which this pitcher plant

occurs. The reasons for diet specialization among carnivorous species remain unclear however

(11).

The extreme example of prey specialization may be found in Nepenthes albomarginata.

As previously mentioned, this tropical pitcher plant consumes only termites and sacrifices a

portion of itself to lure its prey (12, 51). When termites are not available, Nepenthes

albomarginata appears to be a poorly performing carnivorous plant capturing only a few ants,

beetles, and flies during the lifetime of the pitcher. When Nasutitermitinae termites, especially

several species of Hospitalitermes, are present, however, carnivorous success greatly increases

(51).

THE POLLINATORS

Pollination

Carnivorous plants capture a diversity of prey with a variety of different mechanisms but

the process inevitably serves to supplement the acquisition of important nutrients in low fertility

sites (11, 14, 15, 28, 40). These unique plants, however, encounter a precarious proposition when

it comes to attracting prey. Carnivorous species face the conundrum of attracting insects to

27
supplement their nutritional needs these insects must be captured and thereby prevented from

moving away while concurrently attracting insects to transfer pollen from flower to flower or

plant to plant these insects must be allowed to escape the plant in order to ensure outcrossing

(13, 41, 63, 64). This dual role becomes especially problematic when traps and flowers use

similar attractants (13). In order to maximize both prey capture and insect pollination,

carnivorous plants have a variety of mechanisms in place to limit pollinator consumption (12, 13,

63).

Temporal Separation of Flowers and Traps

The most practical way to separate potential prey from potential pollinators seems to be

to separate the traps from the flowers (41). Several mechanisms exist to provide such separation.

Carnivorous plants may differentially place their flowers and traps in time or space or they may

separate traps and flowers by using different lures in an attempt to attract different visitors to each

(10, 41, 63, 65). The oft studied Sarracenia provide several examples of temporal separation. In

S. flava, prey-catching pitchers are not functioning while the plant is flowering (10). Studies of S.

purpurea have shown this species to flower early in the growing season, often ahead of the

production of pitchers. This reduces the likelihood of pollinating insects becoming prey (66, 67).

The butterwort Pinguicula vallisneriifolia, too, has a flowering window in May and June just

before carnivory intensifies in July (41). Early flowering, however, can be reproductively risky.

Sarracenia purpurea may not flower every year possibly because late frosts sometimes kill

developing buds before blooming can occur (8). The flowers may also appear before a reliable

source of pollinators is available thereby precluding cross-pollination (67).

Aside from simply keeping pollinators away from traps, carnivorous plants may time

their flowering for other reasons as well. Carnivorous plants can maximize pollination by

flowering when pollinators are most readily available the more pollinators that may potentially

visit flowers, the greater the likelihood of cross-pollination. Similarly, carnivorous plants may

flower at given times to reduce competition for pollinators from other flowering plants (8, 44, 66,

28
67). Production of blooms when climate is conducive to efficient flower production and when

pollinators are present in sufficient numbers may be as important as avoidance of overlapping the

timing of flowers and traps (8, 66). For instance, some Drosera species appear to bloom for a

very limited time. Drosera anglica flowers may be accessible to pollinators for only a few hours

during a single day (44). Although this concentrates the number of floral visits by pollinators and

increases the likelihood of out-crossing within in that narrow window, it could also result in

missed opportunities to reproduce sexually, a potentially more costly situation than the loss of

some pollinators to carnivory (44, 66). Another means of collecting as many pollinators as

possible over a short period of time may be mass, synchronized flowering of carnivorous species.

This method of flowering may be especially important when pollinators are sparse or unreliable

(66). Regardless of whether carnivorous species are using mass flowering or seasonal timing

with respect to reproductive strategy, these mechanisms may provide a means to avoid direct

competition with other anthophytes for limited pollinators. Darlingtonia californica, for instance,

shares its habitat with several species of lilies, orchids, violets, and other wetland plants. Early

flower production may be an effort to flower when sufficient pollinators are present but before

competition for insects becomes too intense (66).

Spatial Separation of Flowers and Traps

Separation of traps and flowers may be accomplished by placing the two dichotomously

functioning structures in locations that will increase the probability of collecting the appropriate

organism (10, 41, 63, 66). Sarracenia purpurea, like many carnivorous plants, spatially places its

traps well away from its flowers (10, 63). This species maintains relatively short pitchers and tall

flowers (1, 11). Like their North American cousins, the tropical pitcher plants Nepenthes lowii

and N. villosa also hold their flowers well above the traps (65). Two possible lines of thought are

used to explain the placement of flowers above traps (41, 63). Research with Darlingtonia

californica suggests this species constructs tall flowers to discourage pollinators from finding the

traps. This would thereby limit competition between flowers and traps for the same resource

29
namely, potential pollinators (66). Another line of thought advocates that upward flower

placement is better explained as a means by which the carnivorous plants put their flowers in a

location most likely to be seen and visited by pollinators (63). As with many non-carnivorous

plants, taller flowers would be within easy access of flying pollinators, irrespective of traps (63,

68). Studies of some Drosera and Utricularia species support the notion that carnivorous plants

with tall flowers and low traps do indeed place flowers in such a way as to intersect the flight

path of pollinators (63). Tall flowers may also be better placed to disperse seeds further distances

from the parent plant (21, 63).

Carnivorous plants need not be terrestrial to use a spatial separation of traps and flowers.

The aquatic bladderworts (Utricularia spp.) typically construct traps below the surface of the

water while flowers extend above the water line. Flying insects can pollinate flowers without risk

of succumbing to the underwater traps (10, 41). Terrestrial bladderworts use a similar mechanism

to accomplish spatial separation. These Utricularia maintain upright flowers but they produce

their traps beneath the soil (63). Another North American pitcher plant, Sarracenia alabamensis,

uses an apparently novel mechanism for spatial separation. Both pitchers and flowers are of

similar heights and occur contemporaneously; spring pitchers, however, bend over during the

flower period possibly as a way to decrease pollinator consumption and increase pollination (10).

Another possible means of promoting pollination through some sort of spatial

arrangement of flowers may be the directional orientation of blooms. Studies of non-carnivorous

plants and a few carnivorous ones suggest that flower orientation may make the bloom more

appealing to potential pollinators (68, 69). By maintaining an east-facing flower, for example,

several factors may arise that could positively affect pollination. Flower temperature may

increase which provides a thermoregulatory aid for insect pollinators (69). Hemipteran

mutualists on Roridula, for example, use the plants flower petals to shade themselves and

prevent their bodies from overheating (45). East-facing flowers may be easier for pollinators to

see either because visual cues are intensified and shading is reduced or because insects are not

30
hindered in their approach by direct sunlight in their eyes (69, 70). Similarly, sun-tracking leaf or

flower arrangements may maximize sunlight which, in turn, increases the rate at which

photosynthesis and growth of floral related parts progresses (69, 71). Any of these results of

heliotropism should encourage visitation by pollinators and increase the occurrence of pollen

movement from carnivorous plants (68). While Wilson (69) did not find a marked improvement

in pollination with east-facing flowers of Drosera tracyi in Florida, other species could benefit

from such an arrangement.

Other Means of Isolating Pollinators and Prey

Temporal or spatial separation of traps and flowers is not a characteristic of all

carnivorous plants (10, 11, 13, 45). When flowers and traps show little or no separation in timing

of production or spatial distribution, some other mechanism for limiting pollinator consumption

may be in place (10, 13, 45, 65). As with much of the area of carnivorous plant-pollinator

interactions, however, few investigations have been preformed thus far. Various unidentified

mechanisms to separate prey and pollinators probably exist though (10, 12, 44, 65, 66).

Pinguicula vallisneriifolia, for example, simultaneously manufactures some of its flowers near its

sticky leaves. Any potential pollinator faces the risk of easily becoming prey, a problem for both

insect and plant. The reduction in predation of pollinators appears to be mediated, at least in part,

by the size of insects visiting the plant. Apparently, larger insects are more qualified to move

safely about the precariously located flowers and successfully transfer pollen without becoming

prey (41, 44). Pinguicula species apparently trap a greater proportion of small, non-pollinating

insects including aphids, flies, and mosquitoes while larger pollinators such as beetles and

bumblebees are less likely to become stuck to mucus-coated leaf traps. Removal of small insects

may provide a double benefit for some carnivorous plants; they gain a meal and simultaneously

inhibit poor-quality pollinators that would provide little or no reproductive advantage to the plant.

Under such circumstances, trap-flower competition may actually improve both carnivory and

pollination (41).

31
 When influencing carnivorous plant pollination, size specialization appears to be

regularly coupled to environmentally controlled plant quality (41, 46, 63). Abiotic factors such as

the amount of sunlight can lead to poor quality traps ones from which larger insects can easily

crawl free (41, 63). Zamora (41) found that Pinguicula vallisneriifolia size preference was

significantly influenced by the quality of trap mucilage; in turn, mucilage quality declined as

shade increased. Drosera rotundifolia traps were 14% less sticky when grown in shade which,

again, could affect the size class of pollinators (40). Inorganic nutrients can similarly affect trap

quality and indirectly control the separation of pollinators and prey into size classes (30).

Availability of insect prey or soil nutrients can induce higher quality mucilage and favor larger

insects such as pollinators in a sticky flypaper trap species like Pinguicula vallisneriifolia (28).

An even more precise prey specialization may help carnivorous plants separate the

pollinators from the prey (10, 41, 63). Carnivorous species such as Sarracenia psittacina, S.

minor, and Brocchinia reducta prey almost, if not entirely, on ants. Another North American

pitcher plant, Sarracenia leucophylla, preys heavily on moths (10, 15). As long as some other

insect or guild provides pollination services, specialized feeders can maintain both effective out-

crossing as well as carnivory. And the carnivorous plants may not be the only determinant in

keeping potential pollinators away from traps. Some pollinating insect species may simply be too

smart to fall victim to a plants traps. Smart insects would avoid trap danger and be better

potential pollinators (63).

Carnivorous Plant Floral Design

Aside from the need to avoid consuming ones pollinators, carnivorous plants are similar

in floral morphology and functioning to other anthophytes (11, 21). To attract pollinators,

carnivorous plants use a variety of means such as showy flowers or floral patterns, appealing

odors, nectar, or other rewards such as pollen (13, 41, 45, 65, 66). Flowers and traps often use

very similar contrivances to attract pollinator and prey. Studies of Nepenthes alata, Pinguicula

gypsicola, P. zecheri, and Utricularia sandersonii have shown that these carnivorous plants use

32
ultraviolet patterns to attract pollinators to flowers but traps in some species have similar patterns

(13, 48). Comparably constructed flowers and traps, however, use dissimilar shapes, sizes, and

pattern contrasts to separate and herd pollinators and prey to their proper encounter (13). Odors

emitted by flowers and traps could differ as well; for instance, sweet scents from flowers could

attract pollinators while putrid smells could lure carrion feeders to traps. Not all carnivorous

plants use different odors though. Kaul (65) found similar nectaries in both the flowers and traps

in Nepenthes lowii and N. villosa.

Rewards, as with the flowers of many non-carnivorous species, may provide a reliable

means to steer pollinators aright. The flowers of Sarracenia species offer a nectar reward to

pollinators that enter the flowers while prey may be fooled into pitchers by the colorful patterns

and accidentally fall to their doom (11, 67). In Drosera, the presence of nectaries varies among

species suggesting that the genus has assorted mechanisms for pollinator attraction including

floral rewards. Some Drosera apparently offer oils to pollinators but oils can be expensive to

produce by the plant (45). Nectars need not be pleasingly fragrant. In two Nepenthes species (N.

lowii and N. villosa) of Borneo, nectar gives the flowers a foul stench indicative of plants that rely

on pollinators such as some flies and beetles (21, 65). These Nepenthes species also have floral

nectaries that fill with tannins once flowers are pollinated (65). Such flowers could be fashioned

as such to re-direct pollinators away from flowers and thereby be more likely to become prey

once pollination is completed (sensu 41).

Insect Pollinators

All known carnivorous plants are anthophytes and many apparently require some type of

insect pollinator (44). While insect pollination appears to be very important to sexual

reproduction among most carnivorous species, the reproductive biology of carnivorous plants has

rarely been studied (10, 12, 44, 66). Identification of specific pollinators of carnivorous plants

often remains a mystery, too, and even determining the type of pollinator can be problematic (44,

66). One example of this paucity of information concerning pollination in the carnivorous plants

33
comes from the examination of Darlingtonia californica. This species has been studied for a

century-and-a-half and although insect pollination is suspected, an actual insect pollinator has yet

to be identified (66). Insects have been declared to be the only means of pollen transfer among

carnivorous plants by some researchers while others have postulated that spiders may be

important (29, 44, 65). Wind pollination has been advanced for some carnivorous plants such as

species of Nepenthes and Drosera (44, 65). Even birds are implicated as possible pollinators

because some are regular visitors to species such as Drosera macrantha ssp. macrantha and may

transfer pollen between flowers (44).

Regardless of the means of pollination, transferal of pollen is imperative to the long-term

success of plants. In the case of insect-vectored pollination, this becomes problematic if the

plants capture the very organisms required to aid in sexual reproduction (10). Many carnivorous

species are self-compatible but this is only a temporary solution (72). Carnivorous plant species,

like most organisms must be able to reproduce sexually in order to increase genetic variability

and increase the likelihood of prolonged survival (13, 68). Floral characteristics of most

carnivorous plants seem to indicate that many use some animal pollinator (13). While many

Drosera species lack nectar glands to offer rewards for potential pollinators, removal of petals

from flowers resulted in a decline in fruit set suggesting a visually-inclined pollinator was

necessary for maximum reproductive success. (45). Further, research into Darlingtonia

californica showed a reduction in reproduction (fewer mature fruits with individual fruits

containing fewer seeds) when potential pollinators were prevented access to flowers (66). Studies

of Drosera and Roridula imply pollination and seed set are somewhat dependent on insects.

Thrips improved seed set in Drosera while hemipteran pollinators have been identified for

Roridula (45). Sarracenia species apparently require insect-aided cross-pollination to ensure

successful seed set as well (8).

At least six orders of insects (Coleoptera, Diptera, Hemiptera, Homoptera, Hymenoptera,

and Thysanoptera) represented by several dozen families are thought to pollinate carnivorous

34
plants (26, 41, 44, 45). Some carnivorous groups rely on a single set or narrow range of

pollinators. Roridula greatly depend on hemipteran pollinators; R. dentata, for example, gains

two-thirds of seed set from the hemipterans (26). Drosera species, on the other hand,

predominately depend on insects from several families in the Diptera, Hemiptera, and

Hymenoptera (44, 45). Often, insects appear to be limited in their movement among the flowers

of carnivorous specie,s which could lead to a limited number of potential pollinators as well as

little pollen movement (41).

Simply because an insect visits a flower of a carnivorous plant does not mean the insect is

a pollinator. An insect must be available during a species blooming period and it must be

capable of transferring viable pollen from one flower to another (44, 68). An absence of insect

visitors to flowers may be due to a lack of interest for reasons such as a scarcity of nectar or other

rewards or due to competition with traps (44, 63). Potential pollinators can fall prey to

insectivorous predators lurking in the flowers of carnivorous plants, too. In a study of

Darlingtonia californica, Elder (66) found spiders in virtually every mature flower and these

predators took many visiting insects as prey. Spider-captured insects could have been pollinators

of Darlingtonia and their loss could have led to a subsequent reduction in pollination.

Conversely, spiders living among the flowers of some carnivorous species may serve as

pollinators as they move from bloom to bloom. Investigation into this line of reasoning remains

to be completed (29). Even insects that spend extensive amounts of time moving among flowers

do not guarantee pollination. Hemipterans in the family Miridae, for example, apparently feed on

pollen of some Drosera species when the insects are young (45). This could thereby reduce the

reproductive potential of the carnivorous plant.

Self-compatibility and Vegetative Reproduction in Carnivorous Plants

Self-compatibility, a condition found in many carnivorous plant species, is another

possible short-term solution to the predator-pollinator conflict (8, 11, 29, 44). Self-pollination in

some Drosera species, for example, apparently sustains populations of these carnivorous plants

35
through times when insect pollinators are not present (44). Whether because of a general

shortage of possible insect pollinators, inadequate flower visitations, or the loss of potential

vectors to traps, self-fertilization appears to be an important reproductive strategy among some

carnivorous species (45). Even species that appear to be insect-pollinated such as Darlingtonia

californica may depend on self-fertilization until rare pollinators visit (66). Some species that

self-pollinate may still be dependent on insect vectors for movement of pollen from anther to

stigma within a given flower and thereby show facilitated self-compatibility. Anderson et al. (72)

found a reduction in self-pollination when Pameridea bugs were not present on Roridula flowers.

When Pameridea were present, R. dentata showed a 68% fruit set while R. gorgonias had 25%

fruit set. Pameridea, however, seldom move from one flower to another and thereby severely

preclude cross-pollination (17, 72). In Drosera anglica, seed set and seeds per fruit from self-

pollination were comparable to that afforded by insect vectors. Findings such as these apparently

indicate autogamy as the primary reproductive strategy among certain carnivorous species (44).

Other species such as Darlingtonia californica, although self-compatible, have flowers that

appear to be constructed in such a way as to promote cross-pollination while dissuading self-

pollination (11, 29). Self-compatibility may provide viable offspring but it seems to be

counterproductive to the long-term survival of a species (45, 72). Cross-pollination may be a rare

but necessary event with some carnivorous species, especially those that show facilitated self-

compatibility (45).

Vegetative propagation is an important reproductive strategy for carnivorous plants and

may provide another means for carnivorous plants to lesson pollinator-prey conflicts (64). Most

carnivorous plants tend to be long-lived perennials, often relying on asexual reproduction during

some part of their lives (13, 64). Darlingtonia californica, for instance, depends heavily on

stoloniferous growth to produce new plants (11, 29). Asexual production of tissue is a less

expensive reproductive effort, both with respect to energy costs (manufacturing of pollen, nectar,

flowers, embryos, etc.) as well as time demands to produce a new, mature plant (29). For such

36
plants, the loss of potential pollinators to carnivory may be a boon to the vitality of the plant. The

reduction in possible seed set would be counterbalanced by increased prey capture and, therefore,

a greater nutrient input to the plant. This would promote the long-term survival of the plant and

possibly provide future opportunities for sexual reproduction (13, 63). Vegetative reproduction

may be especially important in carnivorous species that require a longer period of time to reach

sexual maturity; Dionaea muscipula, for example, may take four years to flower (14). In plants

that produce very limited numbers of viable seeds, Nepenthes lowii for example, vegetative

reproduction could somewhat offset such poor seed set (65).

THE PECULIAR PARTNERS

Other Partnerships

Carnivorous plants function in predator-prey relationships with various insects and other

organisms (12, 26, 38, 50, 62). Most, if not all, of these bug-eating machines, however, are

dependent on insects for pollination, too (10, 12, 44, 66). At first glance, carnivorous plants

would appear to be dangerous to an invertebrate visitor unless safe passage can be found to and

from the flowers. As an almost counterintuitive notion, carnivorous plants may provide domicile

and diet for a broad range of inhabitants on the plant and even inside the traps. Table 3 shows a

list of some carnivorous species and their insect symbionts. Symbiotic relationships between

carnivorous plants and insects or other organisms extend from tight mutualisms to sloppy

parasitisms (12, 26, 27).

Hypothetically, any carnivorous plant may have favorable or detrimental mutualistic

relationships with insects. The North American pitcher plants (Sarracenia spp. and Darlingtonia

californica) and tropical pitchers (Nepenthes spp.), however, have yielded much of our

understanding of symbioses surrounding carnivorous plants (11, 37, 38, 62, 73). Liquid inside

pitcher leaves hosts entire microfaunal communities including, but not limited to, bacteria,

protists, rotifers, and insect larvae (17, 37, 38). These aquarium-like communities are not only

37
excellent models of larger ecosystems but may be very important to the functioning of the host

plants (12, 26, 74). For carnivorous genera such as Byblis, Darlingtonia, Roridula, and some

Sarracenia, associated symbionts may be required in order for the plant to gain any nutrition from

captured prey because these groups apparently do not secrete their own digestive enzymes (1, 8,

17, 20, 29). In fact, all known instances of carnivory without host digestive materials require

some arthropod symbiont to aid in the breakdown of captured prey (17, 20). The plant-captured

prey, in many instances, first becomes food for the invertebrate community and then is available

in a reduced form to the host plant (12, 27). And scattered along this food chain, a multitude of

commensal organisms function in a caldron of lively, nutrient-rich soup (8, 37)

General Features of Inquiline Communities

Aside from pollination needs, other mutualisms are apparent, common, and relatively

well-studied in Sarracenia, Darlingtonia, Nepenthes, and Roridula genera that all appear to

lack the ability to digest their prey actively (8, 17, 18, 20, 25). Each of these genera has a major

symbiotic species or group of species and a plethora of less common but highly important

symbionts. In pitcher plants such as the Sarracenia, inquilines those organisms living in the

pitcher make up entire communities that generally consist of several trophic levels (38, 52, 62,

74, 75). The base trophic level inside pitcher leaves is comprised of various bacteria that support

several groups of bacterivores including protozoans, rotifers, and several species of insect larvae

(38, 52, 74, 76). Bacteria, along with protists, are the largest contributors to the inquiline biomass

and are highly important to the productivity and nutrient cycling inside pitchers (74). Prokaryotes

break down captured prey and liberate nutrients into the pitcher fluid (8, 74). Nutrients may then

be used by inquiline community members or the plant host (25, 43). Regardless of the

composition and number of species within pitchers, three trophic levels can typically be found in

carnivorous plants such as Sarracenia and Darlingtonia (74). Figure 1 shows a typical

community food web within Sarracenia purpurea pitchers.

38
Table 3 Examples of plant-animal mutualism in carnivorous plants and allies. In Hartmeyer
(17).
Plant Arthropod Occurrence
Byblis gigantea Setocornis bybliphilus Perth, Australia
Byblis liniflora Setocornis/Cyrtopeltis species Kununurra & Cairns, Australia
Darlingtonia Metriocnemus edwardsi. USA
californica
Drosera erythrorhiza Cyrtopeltis droserae, C. russelli Perth, Australia
Drosera pallida Cyrtopeltis droserae, C. russelli Perth, Australia
Drosera stolonifera Cyrtopeltis droserae, C. russelli Perth, Australia
Drosera indica varieties Setocornis/Cyrtopeltis species Kununurra & Darwin,
Australia
Drosera ordensis A tiny Miridae species North Australia
Heliamphora Several mosquito larvae Venezuela
Nepenthes bicalcarata Camponatus schmitzi Borneo
Misumenops nepenthicola
Thomisus nepenthiphilus
Mosquito larvae
Various Nepenthes Several mosquito larvae Asia, Australia, Madagascar,
Seychelles
Roridula dentata Pameridea marlothii South Africa
Roridula gorgonias Pameridea roridulae South Africa
Sarracenia flava Sarcophaga USA
Sarracenia purpurea Wyeomyia smithii USA, Canada

Figure 1 Hypothesized organization of the food web in Sarracenia purpurea pitchers. Very
slightly modified from Cochran-Stafira and Von Ende (74).

Wyeomyia smithii (or another top

predator)
III

Protozoa
II Rotifers such as Habrotrocha rosa

Algae Bacteria Yeast

39
I

Metriocnemus
Detritus Blaesoxipha
Mites

The associated inquiline community appears to be a requirement for carnivory to occur or

at least occur at a sufficiently rapid rate for plants to gain signinficant nutrition from captured

insects (17, 29, 38). Carnivorous plants that house inquilines, therefore, may be seen as

specialists that can utilize carnivory only or predominately through the aid of insects and/or

bacteria (17, 73). This may be especially important with respect to marginal genera like

Brocchinia, Catopsis, and Heliamphora groups that appear to supplement their diets with prey

but lack at least one of the four characteristics deemed necessary to classify a plant as carnivorous

(15, 17).

Bacterial Symbionts

Sarracenia purpurea and other species that lack dissolving enzymes appear to provide

ideal habitat in their pitcher fluids for proteolytic bacteria and, therefore, do not need to produce

their own digestive secretions (8). In carnivorous plant species that do not generate their own

digestive substances, autolytic enzymes of the prey may supplement bacterial exoenzymes in

speeding decomposition and subsequent nutrient availability (8, 38). Bacteria are apparently

especially efficient in breaking down prey particles with large surface area (8). Because of this,

inquiline insect larvae that act as prey shredders interact to aid bacteria-effected decomposition

(20, 52, 74). Consequently, a large presence of bacteria increases food availability for insect

larvae (38, 52).

40
 While proteolytic bacteria may be common in pitchers, other prokaryotic forms also

occur. Although photosynthesis is limited in the inquiline community inside pitchers,

photosynthetic bacteria may be found there (8, 74). Very large populations of purple non-sulfur

photosynthetic bacteria such as Rhodomicrobium have been found in Sarracenia purpurea

pitchers but their role in the inquiline community is not known. Nitrogen-fixing bacteria have

also been isolated from pitchers (8). It is possible that this group increases nitrogen availability to

the host plant but more research needs to be done in this area. Some bacteria found in pitchers

may be incidental. Prey, for instance, may carry intestinal bacteria to pitcher plants where the

prokaryotes would be released during decomposition (8).

Insect Symbionts

The bacterial assemblage is only one part of a pitchers inquiline community. Pitchers

may contain a biologically rich collection of organisms that plants do not consume. Other

inquiline creatures include copepods, crustaceans, nematodes, rotifers, and mites. Sarracenia

purpurea generally provides a nursery for the larvae of three dipterans, too, including the pitcher-

plant mosquito Wyeomyia smithii (replaced by W. haynei in some southern locales), the pitcher-

plant midge Metriocnemus knabi, and the sarcophgid fly Blaesoxipha fletcheri (8, 25, 36, 38, 62,

76, 77). Darlingtonia californica support a similar set of genera with slightly different species;

for example, Metriocnemus edwardsi, a close relative of M. knabi, supplants Wyeomyia as the

dominate inquiline insect of Darlingtonia pitchers (17, 29, 78). Insect larvae may feed on lower

inquiline trophic levels or detritus generated from plant-captured prey (62, 74). Detritus is a

major driving force in inquiline communities because photosynthesizers are limited inside

pitchers and little primary production occurs there (74). Pitcher plant detritus is generated as prey

is shredded by inquiline organisms and communities are, therefore, regulated by the success of

the carnivorous plant in capturing prey (37, 52, 79).

Dipteran mutualists apparently prefer certain pitchers and tend to select those sites for

egg-laying. And even slight edaphic differences can produce uneven colonization events.

41
Pitcher-plant midges, for example, appear to choose pitchers with more fluid while pitcher-plant

mosquitoes may select pitchers of a certain age (80). Plant position within a site also influences

colonization. Pitchers near adult dipteran feeding or mating sites tend to receive more larvae than

those pitchers that are less closely located (77). Some pitchers probably enjoy greater inquiline

insect colonization by simply being more readily accessible, too (76). Even seemingly minor

points of dissimilarity in plant position can lead to significant variations in pitcher microclimate

(76, 77, 80). Pitchers in full sun, for example, may dry out more readily than those in shady sites.

As pitcher fluid dissipates, the inquiline community can be extirpated (80). Similarly, pitcher

temperatures can vary from favorable to lethal for larvae within a small geographic location (77).

Temperature effects on survivorship of larvae is unclear however (77, 81).

Whether across sites or within individual plants, pitcher selection by ovipositing insects

appears to be ultimately a function of potential prey capture in the host pitcher. This, in turn, is

related to the accumulation of organic material (81). Larvae are more likely to survive in pitchers

with sufficient amounts of food and pitcher fluid (80). As pitchers age, they tend to capture more

prey lending to increased larval survivorship in those pitchers. There appears to be an optimal

age to pitchers for insect colonization however (77, 80). Ovipositing pitcher-plant mosquitoes,

for instance, prefer newly produced pitchers to those from the previous seasons growth (80). As

Sarracenia purpurea pitchers age, insect capture rates tend to decline as do dipteran colonization

rates (77). Larger pitcher leaves catch greater amounts of prey and are preferentially selected by

dipteran mutualists (77, 80, 81). Although poorly understood, dipteran females like pitcher-plant

mosquitoes may choose oviposition sites through the use of some chemical attractant found in

pitcher fluids. Characteristics such as hood shape or color do not appear to influence pitcher

selection by these dipterans significantly (80).

Ovipositing pitcher-plant mosquitoes, midges, and flies preferentially prefer pitchers that

will provide their offspring with suitable habitat and sufficient food supplies (77, 80). Following

colonization decisions, microclimate coupled with food availability dictates survivorship of

42
larvae within pitchers (38, 77). All of these factors help promote rich biodiversity within pitchers

across large geographical areas. And contrary to many studied ecosystems, Sarracenia inquiline

communities show a positive correlation between species richness and higher latitudes (37, 68,

81, 82). Selective ovipositing based on temporal or spatial variations among plants or sites also

appears to influence successional changes in inquiline community structure (62). As new pitchers

open and fill with water, the traps are rapidly colonized (37, 62). Studies of Sarracenia flava

have shown that bacteria become established inside pitchers within days of opening. Bacterial

abundance and assemblages then change quickly through time with earlier successional seres

often creating favorable environments for later groups (62). Populations appear to fluctuate as

plant-captured prey is broken down. The greatest abundance of bacteria can often be found

within one to two weeks of the capture of a prey item by the host plant (8).

Insect communities change over time inside pitchers as well. In Sarracenia purpurea, for

example, the numbers of both bacteria and pitcher-plant mosquitoes increase rapidly for about

two to three weeks following production of a new pitcher. After that period, however, the

inquiline community apparently becomes relatively stable and the abundance of organisms as

well as the community structure changes little (37). Pitcher-plant midge populations undergo a

pattern of change, too. Larvae numbers are relatively small in young pitchers, increase as traps

age, then decline as the pitchers move towards senescence (62). Changes in inquiline community

structure are typically related to changes in pitcher functioning and changes in pitcher functioning

are, in turn, related to pitcher age (37, 62, 81). Buckley et al. (37) reported younger pitchers not

only captured more prey but tended to support larger communities of inquiline fauna. As either

plant-captured prey supplies or bacterial populations decline, insect larval populations are

reduced (52). These reported general patterns of temporal inquiline changes are comparable to

more traditionally-studied successional communities such as old-fields or ponds (68, 83, 84).

Contrary to these findings, no clear successional patterns within Sarracenia purpurea pitchers

were observed in northern Florida wetlands (76). Instead, early colonization and stochastic

43
events may have allowed the top inquiline predator to control the abundance of other pitcher

fauna (76, 80).

Although some disagreement exists concerning whether and how much inquiline

succession occurs, community interactions initiated through insect pitcher preferences have a

major impact on community structure inside pitchers (77). Pitcher selection has an indirect but

extremely important effect on inquiline community structure and possibly the level of benefit

these communities provide their hosts. Predation of inquiline members by carnivorous insect

larvae such as Wyeomyia smithii as well as other inter- and intraspecies interactions has a very

significant impact on determining community composition especially with respect to bacteria and

protists (37).

The Sarracenia-Wyeomyia System

While several symbiotic relationships have been described between carnivorous plants

and inquiline community members, probably the best known and best studied is the partnership

between Sarracenia purpurea and the obligate pitcher-plant mosquito Wyeomyia smithii. The

Sarracenia are ubiquitously associated with Wyeomyia spp. which act as keystone predators

within pitchers (37, 38, 49, 52, 62, 74, 76, 79). Wyeomyia larvae are free-swimming filter-feeders

that consume bacteria, protozoans, and suspended particulate matter (37, 52). The number of

larvae varies from pitcher to pitcher but they are typically abundant (37, 52, 76, 80). In

Sarracenia purpurea pitchers, Nastase et al. (80) and Miller et al. (76) have reported similar

numbers of Wyeomyia smithii larvae in pitchers an average of 17 and 20.7 larvae per pitcher,

respectively. Southern populations of this pitcher plant species, however, can contain 80 larvae

per pitcher (52). Wyeomyia populations are limited by the amount of plant-captured prey

available in a pitcher (76, 81). When prey are readily available, Wyeomyia densities increase but

both abundance and diversity of other inquiline species decreases (81). The relationship between

Wyeomyia and Sarracenia is somewhat unclear. Pitcher-plant mosquitoes could be commensal,

simply living off of abundant bacteria and protists in pitchers, or the larvae could speed the

44
release of nitrogen to the carnivorous plant by limiting bacterial growth and the concomitant tying

up of nutrients in prokaryotic biomass (25, 38). Sarracenia may also benefit from Wyeomyia by

using the larvae as a lure predacious insects seeking to feed on Wyeomyia can slip into the

pitcher fluid and become prey (25). Similarly, an adult Wyeomyia could drown during

oviposition and provide sustenance to both her offspring as well as the carnivorous plant. Larvae

that do not survive also become prey (sensu 62). It is also possible that Wyeomyia or another

dipteran symbiont may serve as a pollinator for Sarracenia (8, 25).

Wyeomyia larvae heavily influence community structure inside Sarracenia pitchers and

can significantly reduce the number of other inquiline species (81). Yet, Wyeomyia shares a

given pitcher with not only bacteria, protists, and several less common species but typically one

or more larvae of pitcher-plant midges such as Metriocnemus knabi and sarcophagid flies like

Blaesoxipha fletcheri (8, 38, 62, 76, 80). In a Sarracenia purpurea pitcher, W. smithii, M. knabi,

and B. fletcheri all consume some portion of plant-captured prey or other inquiline members (74,

80, 81). Competitive exclusion, however, does not occur because resources are partitioned

among the three species (52, 62, 75). The dipteran larvae have dissimilar feeding habits and

consume different-sized food particles (74, 81). Both B. fletcheri and M. knabi, for example, feed

on insect carcasses in the pitcher fluid. Blaesoxipha fletcheri larvae, however, take recently

captured prey near the surface of the pitcher liquid while M. knabi larvae favor insect bodies that

have settled to the bottom of the pitcher (38, 62). Some competition could occur between M.

knabi and B. fletcheri but spatial segregation of prey as well as temporal separation of pitcher use

limits competitive interactions (62, 75). Blaesoxipha fletcheri tend to colonize pitchers earlier

and metamorphose to adults sooner than M. knabi. This temporal disparity in pitcher use also

allows each species greater access to their preferred food type. Fresh, floating prey is more

common in younger pitchers while older prey items are readily available in the bottom of older

pitchers (62). Wyeomyia smithii appears to benefit from the presence of M. knabi when both

dipteran larvae occur together (62, 75, 81). Metriocnemus knabi shreds its prey while feeding

45
(52). Although M. knabi takes some prey that Wyeomyia would otherwise consume, shredding

increases particulate matter in the fluid which leads to higher bacterial and protozoan populations

and, in turn, the filter-feeding Wyeomyia have access to more of its food sources (52, 62).

Metriocnemus knabi also benefit their carnivorous plant hosts. The midge larvae act much like

shredders in stream ecosystems, breaking larger particles into sizes that can be better used by

neighbors (20). As plant-captured prey is broken into smaller pieces, bacteria have more surface

area to speed digestion. Bacterial action, as well as defecation by insect larvae feeding on various

sized particles, releases nitrogen and other elements into the pitcher fluid allowing the plant to

absorb the nutrients (25, 52, 62, 81). Mites (Sarraceniopus gibsoni) also occupy Sarracenia

pitchers but their role in the infaunal community remains unclear (77).

Darlingtonia-Inquiline Symbioses

While the Sarracenia-Wyeomyia system and its associated inquiline organisms are

relatively well-known, other such mutualistic and commensalistic interactions exist among

carnivorous plant species. A very similar community occurs in the pitchers of Darlingtonia

californica and much like Sarracenia many inquiline organisms, the infauna of Darlingtonia are

facultative but mostly restricted to this specific carnivorous species (29). Midges, for instance,

are found in both Sarracenia and Darlingtonia but Metriocnemus edwardsi favors Darlingtonia

while M. knabi is associated with Sarracenia (29, 38, 80). While both of these pitcher plant

genera have mites in their infauna, mites seem to play a larger role in the Darlingtonia inquiline

community (29, 74, 75). Pitcher-plant slime mites (Sarraceniopus darlingtoniae), M. edwardsi,

and Darlingtonia interact in a manner similar to the Sarracenia-Wyeomyia-M. knabi relationship

(38, 62, 75). Darlingtonia midges act as shredders of plant-captured prey items (75). Breakdown

of prey along with excretion of nitrogenous wastes by M. edwardsi increases the release of

nutrients to the host plant (38, 75). Mites may further degrade prey particles but, as in

Sarracenia, their role in the host nitrogen budget is poorly understood (29, 75). It is possible that

46
S. darlingtoniae robs the carnivorous plant of some nitrogen but their small biomass within

pitchers apparently negates much host loss (75).

Darlingtonia californica and their midges, mites, and bacteria are more likely

mutualistic. The invertebrates along with the bacteria are provided a safe habitat and a ready

food supply while the carnivorous plants receive greater nutrient input from the prey they have

caught (29, 52). This is important with Darlingtonia because this species apparently lacks

digestive enzymes (11, 12, 29). Competition increases between Sarraceniopus and Metriocnemus

when mite populations are large and plant-captured prey is in short supply (77). When prey is

abundant, mites and midges successfully coexist because resources are partitioned in both time

and space. (75, 77). Metriocnemus edwardsi feeds on fresher prey insect parts while

Sarraceniopus darlingtoniae colonizes older carcasses. The mites also appear to consume slime

presumably generated by bacterial and protozoan action during decomposition of prey insects

(75).

The Nepenthes bicalcarata-Camponotus Ant Symbiosis

The tropical pitcher plant Nepenthes bicalcarata serves as a symbiotic partner, too, with

specific insect inhabitants (2, 26, 38, 64, 73). Camponotus ants are found almost exclusively in

N. bicalcarata and appear to function in a relatively tight mutualism (73). When Clarke and

Kitching (73) originally studied the N. bicalcarata-Camponotus system, the ants were of an

undescribed species. Hartmeyer (17) more recently classified the species as Camponatus

schmitzi. Because of the discrepancy in nomenclature, the ants will be identified as Camponotus

here. In this symbiosis, the ants chew holes into the plants hollow tendrils and nest there (12,

73). Along with shelter, ants take large drowned prey from pitchers by diving into the trap fluid

(73). Host plants also benefit from this relationship. Large prey items are broken into smaller

pieces thereby speeding the digestive process (26, 61, 73). The feeding behavior of the ants

prohibits excess accumulation of prey and potential plant damage (26, 38, 73). Nepenthes

bicalcarata pitchers can become clogged with large prey causing the plant tissue to decay (73).

47
 Camponotus ants not only aid the Nepenthes host but co-occurring fauna as well.

Without Camponotus, the inquiline communities would be lost as clogged pitchers rotted.

Camponotus ants further benefit their faunal neighbors and plant hosts indirectly by slowing

decomposition by bacteria. Pitcher plants, whether Nepenthes or Sarracenia, release oxygen into

pitcher fluid (38, 73). During decomposition of prey, bacteria can use up oxygen supplies within

the pitcher liquid thereby undermining their own population success as well as that of other

infauna (26, 38, 73). If, however, oxygen levels are maintained at sufficient levels, the inquiline

community continues unabated in the breakdown of plant-captured prey and the plant benefits

from the subsequent release of nutrients (73).

Ants are also found on the surfaces of Sarracenia. The relationship between ants and

North American pitcher plants is a bit murky. Ants take nectar from pitchers, which constitutes a

loss of resources; however, the plants capture some ants adding to nutrient budget of the

carnivore. The cost versus benefit of ants to Sarracenia has yet to be clearly elucidated (27).

Roridula-Pameridea Interactions

Pitchers of Sarracenia, Darlingtonia, Nepenthes, or some other pitfall-trap carnivorous

species provide safe haven, if the harsh and dangerous environment can be overcome (2, 17). For

an insect or some other organism to live in water-filled pitchers, it must be able to withstand

relatively hostile digestive enzymes produced by the carnivorous plant host or other organisms in

the soup. To avoid being digested themselves, these organisms are generally characterized by

features that allow them to reside safely in a habitat that is comparable in some ways to a stomach

(2). The larvae of insects like flies in the Sarcophaga secrete substances that work as antagonists

to the digestive enzymes surrounding them (11). Other inquiline members may spend only a

portion of their time in the digestive bath (2, 73). Regardless of the mechanism, these symbionts

find themselves living, if not in the belly of the beast, at least in its mouth. But carnivorous plant

symbioses need not occur only within pitchers. Commensal pseudoscorpions, for example,

inhabit leaf surfaces of carnivorous bromeliads (15). Various ant species spend considerable

48
amounts of time traversing the leaves of sticky-flypaper trap species such as Drosera and either

indirectly aid in plant digestion or steal prey from the host (12, 85).

The mutualism between Roridula and Pameridea is a very significant symbiosis. Studies

of Roridula species have shown that these carnivorous plants rely very heavily on hemipterans in

the genus Pameridea for most of their nitrogen budget (20, 26, 45, 86). Roridula is another

carnivorous genus that fails to produce its own digestive enzymes (17). Nor does it have pitcher

traps filled with bacteria to dissolve insect proteins into plant-available nitrogen. Instead, sticky

leaf traps are used to ensnare insects (1, 20, 26, 52, 74). Those prey items would remain useless

to the plant if it were not for the small hemipterans living on the plant (20, 26). Pameridea

species walk safely among the sticky leaves feeding on plant-captured prey (26). While foraging,

the Pameridea defecate onto the leaves of Roridula and the plants appear to absorb the nitrogen

through their stomata (17, 26). In so doing, Roridula may receive nearly three-fourths of its

nitrogen from the hemipteran feces, an amount comparable to some of the most prey-dependent

true carnivorous plants (26). For example some Drosera gain about 68% of their nitrogen from

insect prey and Dionaea about 75% (20). Both of these species have each of the four traditional

characteristics of carnivorous plants as defined by Givnish et al. (15). Darlingtonia, a species

characterized as carnivorous but apparently lacking plant-secreted digestive enzymes receives

76% of its nitrogen from capture prey (20). The Roridula-Pameridea symbioses appear to be

highly mutualistic and species-specific among different plants and bugs within the genera (20, 26,

45). Pameridea not only provide large amounts of nitrogen to their symbiont hosts but may also

act as pollinators of Roridula, further extending the mutualism between these two groups (45).

Other Carnivorous Plant Symbioses

As work on carnivorous plants progresses from the descriptive stage to more ecological

work, findings indicate that interactions among plants and non-prey organisms are relatively

common (2, 12, 14). And some of the partnerships seem truly unique. Nepenthes lowii, for

example, depends on animal feces deposited into pitchers to supplement carnivory. Unlike the

49
Roridula-Pameridea bug symbiosis, N. lowii receives nitrogen from sunbirds in exchange for

nectar-like exudates (12). The bladderwort Utricularia purpurea appears to favor the capture of

green algae in traps that do not function in carnivory. In lieu of consuming these organisms, the

algae are kept as mutualistic partners. Plants gain resources from their symbiont while the algae

are provided safe haven (12, 14). Some Nepenthes and Sarracenia also have green alga in their

pitchers and these relationships may prove to be mutualistic as well (14, 76).

Carnivorous plants have a wide variety of mutualistic relationships; however, most

typically do not have mycorrhizal associations (8, 59). Mycorrhizal fungi generally aid their host

in acquisition of nitrogen and phosphorus and, in turn, receive carbon from the plant (7, 87, 88,

89). Aquatic, semi-aquatic, and wetland plants, however, generally lack mycorrhizal symbioses,

possibly because inundated roots offer poor habitat for the fungi (7, 68, 87, 88). Because a large

number of carnivorous species grow in wetland soils, mycorrhizal associations may be of little

ecological value for the fungal symbiont. The majority of carnivorous plants have meager root

systems, too (13). Carnivorous plants, therefore, may serve as poor mycorrhizal partners.

Carnivory may serve to provide additional nitrogen or phosphorus that most plants receive via

mycorrhizas (sensu 59).

When a mutualistic relationship does occur between a carnivorous plant and one or more

other species, the plant generally obtains nitrogen, phosphorus, or some other essential nutrient

(10, 25, 38). The animals, protists, or bacteria generally receive a habitat relatively safe from

many predators because traps are dangerous places to search for food (2, 90). Mutualistic

organisms found among carnivorous plants have access to a stable supply of food items, if the

symbiont can effectively overcome the hosts trapping mechanisms (38, 73, 81). Some

organisms, however, not only overcome the trap but cheat the system (2, 8, 11, 17, 26, 61).

Robbers, Cheaters, and Other Crooks

Aside from the apparently minor losses of nutrients to commensal or mutualistic

symbionts, carnivorous plants may compete directly with invertebrates or even vertebrates for

50
insect prey (2, 10). Some ants are able to move freely about Drosera trap leaves stealing plant-

captured prey (17). Drosera as well as Byblis suffer theft at the mouthparts of capsid bugs such

as Cyrtopeltis and Setocornis (1, 12). Loss of prey to marauding insects and spiders may lead to

carnivorous plant characteristics designed to reduce parasitism. Drosera, for instance, may

rapidly and tightly wrap their prey as much to prohibit theft as to hold the victim (12). Nepenthes

ampullaria suffer a loss of prey as the crayfish Geosesarma malayanum forages in their pitchers

(17). Even frogs apparently steal prey from Sarracenia pitchers on occasion (10). And prey

robbers can apparently take a significant amount of prey from carnivorous plants (26).

Spiders seem to be especially kleptomaniacal or competitive (2, 37, 61, 66). Crab spiders

forage on insects recently captured by Roridula and Byblis (1). Dozens of species of Nepenthes

provide habitat and easy pickings for other crab spiders such as Misumenops nepenthicola and

Thomisius nepenthephilus (2, 12). These spiders will dive into pitchers for prey. Adult and

juvenile spiders also hide in the pitcher fluid from potential predators and may remain there for

up to forty minutes (2). Spiders will also interfere with mutualistic relationships. In the

Roridula-Pameridea symbiosis, for example, spiders prey on the hemipterans. This reduces the

amount of nitrogen released to the carnivorous plants by the Pameridea. The spiders, conversely,

fail to return much nitrogen to the plant (26). Predation by free-roaming spiders not only limits

plant nutrition but may negatively influence reproduction directly through attacks on pollinators

(2, 66). Web-building spiders compete with carnivorous plants, too. Cresswell (61) found that

nearly one-third of Sarracenia purpurea pitchers were blocked by spider webs and pitcher plants

lost significant potential prey to the spider inhabitants.

Most of these invertebrates exemplify a potential problem in declaring a carnivorous

plant prey robber simply a competitor or kleptoparasite. Much like the relationship between

Roridula and Pameridea, ants, capsid bugs, spiders, and crayfish may convert inaccessible

nutrients from the body of plant-captured prey into feces and, hence, nutrients that can be

absorbed by the plant (12, 17, 20, 26, 85). Thieves may be sloppy eaters, too. As they crush or

51
shred their ill-gotten gain, the prey is broken into smaller pieces that will more rapidly decay in

the presence of bacteria to plant-available nutrients (2, 12, 85). The reduction in prey brought

about by robbers may aid carnivorous plants by preventing clogging and rotting of traps. Thieves

may, therefore, serve an important housekeeping role for the carnivorous plant (73, 85). Prey

robbery can be a deadly game to the thief but a beneficial one to the host. While trying to

capitalize on the work of a carnivorous plant, a robber, cheater, or parasite can become the

plants next meal (2, 80). Even when insects are obviously prey items, the relationship between

plant and animal is questionable. Because so few insects are captured, at least in some

carnivorous species, the potential prey may gain a reward many times before succumbing to the

predacious plant. Some suggest this reflects a mutualism even between insect prey and

carnivorous plant (29). It is also possible that carnivorous insects or spiders could decrease

predation of the plant by herbivorous invertebrates. If spiders, for example, feed on insects that

would damage the carnivorous plant, the loss of potential prey to the plant may be offset by the

protection afforded it by the prey robber (sensu 90, 91).

To borrow generously from an old song, bad guys will be good guys and good guys will

be bad guys on occasion in the mixed up, messed up world of carnivorous plants. Mutualists may

take some plant-captured prey from the host but increase availability of the remaining nutrients in

the process (26, 74, 75, 79). On the other hand, prey robbers may provide important services to

their hosts by removing excess prey or balancing bacterial populations (2, 73). But some

organisms associated with carnivorous plants do appear to be entirely problematic for the plants.

North American pitcher plants, for instance, may become infested with cricket-hunting Isodontia

wasps. These insects damage the traps and reduce the prey captured by carnivorous plants (8,

11). Isodontia wasps fill pitchers with grassy nests and prey they have taken for their young

thereby rendering the pitchers useless for carnivory (11). The larvae of Exyra rolandiana moths

damage Sarracenia purpurea pitchers, too. After oviposition by the adult female, the larvae clog

the pitcher before consuming the trap tissue (8). Birds may compound the damage to infected

52
pitchers. Upon discovering a pitcher containing Exyra larvae, birds that have learned to do so

poke holes into the trap in search of their prey (11). Insects that would become prey items may

damage carnivorous plants, too. Large insects such as bumblebees (Bombus spp.), for example,

may chew through pitchers and, in the process, drain the digestive fluid as the liquid leaks out

(61). Sarracenia plants can suffer considerable damage from larvae of the root borer Papaipema

appassionata (11). Other pests and parasites are bound to harass carnivorous plants as well.

FINAL THOUGHTS

Future Thoughts

After several centuries of observation, detailed study, and increased understanding, our

knowledge of carnivorous plants continues to grow. The future looks to offer a great deal of

opportunity for further investigation and insight into these amazing plants. Seemingly simple

questions remain to be answered. Who really pollinates Darlingtonia californica or many other

carnivorous species for that matter (29)? Do plants such as Sarracenia purpurea or Brocchinia

reducta aid in the digestion of their prey (15, 25, 38)? What molecular mechanisms are involved

in the absorption of nutrients following prey digestion (12)? How do carnivorous plants respond

to a combination of edaphic conditions such as drought and nutrient availability (13)? What are

the overall costs imposed on carnivorous plants by their symbionts (26, 27, 73)? How might

increased nitrogen deposition affect carnivorous plant growth and competition with non-

carnivorous plants (13, 43)? Could carnivorous plants cause a reduction in sexual reproduction of

neighboring plants by capturing their pollinators? If this were the case, would carnivorous plants

have an even greater ecological advantage over their non-carnivorous neighbors? Similarly,

assuming autogamy is a normally viable reproductive strategy, could pollinator attraction be more

about potential prey attraction?

Carnivorous plants provide excellent opportunities to model larger systems. With three

trophic levels within a single Sarracenia purpurea pitcher, for instance, broad ecological

53
concepts can be observed and manipulated within a confined system (74). As the study of

carnivorous plants catches up with new research already being done with non-carnivorous

species, even greater ecological knowledge may be added to our understanding of carnivorous

plants. Communication between herbivore-injured carnivorous plants and carnivorous insects,

for instance, may prove to be a highly complex but fascinating system to study (91, 92, 93, 94).

Under such circumstances, carnivorous plants would attract three types of organisms: prey,

pollinators, and anti-herbivory arthropods (sensu 95). Would carnivorous plants have to avoid

not only eating their pollinators but also their carnivorous insect rescuers?

Carnivorous plants stand out in an ecosystem in an effort to attract prey actively as well

as pollinators. Herbivorous insects may find most plants by using volatiles released from foliage

or flowers (91). Because carnivorous plants are apparently so obviously visible to organisms

for the entirety of the growing season, the plants may be more readily seen by herbivores as

well as prey. Carnivorous plants could, hypothetically, attract their own nemeses more

effectively than non-carnivorous plants. If one can find them and avoid the pitfalls or bear traps

or sticky flypaper, carnivorous plants might provide excellent safety and sustenance. It is

possible that herbivores or prey robbers could specialize in search and destroy raids on

carnivorous plants using chemical cues released by the plant to attract prey.

Strange World

Carnivorous plants are unique organisms in a world filled with uniqueness. The ultimate

appeal for many researchers and layman to carnivorous plants has been the strange ability to

attract, capture, digest, and absorb prey (12, 15). Carnivorous plant species have a variety of

traps to take their meals and the traps are beautifully designed to befuddle insects and other

organisms (13, 48, 50). Carnivory provides these plants the opportunity to exploit habitats that

may not be conducive to many non-carnivorous plants (13, 15). When an ecosystem offers high

light, consistent moisture, low soil nutrients, and abundant insect prey, carnivorous species seem

to be the plants to beat. And they hold their own quite well in such competition (12, 29).

54
 Although carnivorous plants stand to gain a great deal through carnivory, they face a

serious dilemma, too. Carnivorous plants require insects and other organisms as prey. Insect

pollinators are also apparently required by most, if not all, carnivorous plant species (10, 63). At

least some carnivorous plants compete with themselves for a potentially limited number of

insects. Traps may reduce the number of pollinators available to a carnivorous plant as insects

are taken as prey. When insect pollinators safely transit a carnivorous plant to and from flowers,

potential prey items are lost (13, 63). How does one use a similar resource to accomplish two

diametrically opposed tasks? Many plants appear to have mechanisms in place to help reduce the

probability of consuming pollinators a means to avoid eating ones future (10, 30, 72). Spatial

or temporal separation of traps and flowers, preferential pollinator-size selection, and greater

reliance on vegetative reproduction aid carnivorous species in overcoming the problems of

competition within ones self for resources (10, 41, 60, 63).

In a seeming contradiction to the concept of carnivory, a plethora of bacteria, insects, and

other organisms enjoy symbiotic relationships with carnivorous plants (26, 52, 73, 74, 80). The

spectrum of interactions extends from mutualist to predator. To quote that ecological crooner

Steve Perry, some will win, some will lose, and some are born to sing the blues. Mutualists,

commensalists, parasites, and other predators all interact in, on, and around and the distinctions

between these relationships are often hazy (2, 26, 80). A significant number of carnivorous plants

appear to digest their prey much more efficiently through the aid of their symbionts (17, 38).

Other carnivorous plants might not even be carnivorous if their mutualists were unavailable (20,

26). Whether walking through a jungle of sticky flypaper mucilage or swimming through an acid

bath within pitchers, parasites and predators are able to skirt the traps and defenses of carnivorous

plants and exploit these relatively hostile environments (2, 11, 26, 73). From ants to spiders to

wasps, the plants that turn the table on animals (10) may, in turn, have the table turned back.

Our knowledge of carnivorous plants and their interactions with a wide range of life

forms has grown tremendously over the centuries. Due to the uniqueness and complexity of

55
carnivorous plants and their ecology, questions abound when studying these organisms. But

whether capturing prey, using pollinators, sharing with mutualists, competing with robbers and

cheaters, or confounding researchers, these approximately six hundred species of plants deserve

the attention they have received and much to come.

Kingdom Plantae has yet other devious machinery to use against

Animalia.

Barry Rice (12)

Literature Cited
1. Lloyd, F.E. 1942. The Carnivorous Plants. Chronica Botanica, New York.

2. Pollard, S.D. 2005. Bugs in jugs. Nature Australia 28(4):68-69.

56
3. Conant, R. and J.T. Collins. 1991. Peterson Field Guides: Reptiles and Amphibians
(Eastern/Central North America). Third Edition. Houghton Mifflin Company. Boston.

4. Barnes, R.D. 1980. Invertebrate Zoology. Fourth Edition. Saunders College. Philadelphia.

5. Ruppert, E.E. and R.S. Fox. 1988. Seashore Animals of the Southeast. University of South
Carolina Press. Columbia, S.C.

6. Thorn, R.G. and G.L. Barron. 1984. Carnivorous mushrooms. Science 224: 76-78.

7. Alexopoulos, C.J., C.W. Mims, and M. Blackwell. 1996. Introductory Mycology. Fourth
Edition. John Wiley and Sons, Inc. New York.

8. Lindquist, J. Bacteriological observations on the leaves of Sarracenia purpurea

http://www.splammo.net/ppproj/cpmicro.html

9. Anonymous. 2002. Malaria. U.S. Department of Health and Human Services. National
Institute of Allergy and Infectious Disease.

10. Mellichamp, L. Carnivorous plants and their prey. http://gardens.uncc.edu/carnivorous.htm

11. Schnell, D. 1976. Carnivorous Plants of the United States and Canada. John F. Blair Press.
Winston-Salem, N.C.

12. Rice, B. 2002. Carnivorous plants classic perspectives and new research. Biologist 49 (6):
245-249.

13. Ellison, AM. And N.J. Gotelli. 2001. Evolutionary ecology of carnivorous plants. Trends in
Ecology & Evolution 16(11): 623-629.

14. What is a carnivorous plant? http://www.sarracenia.com/faq.html

15. Givnish, T.J., E.L. Burkhardt, et al. 1984. Carnivory in the bromeliad Brocchinia reducta,
with a cost/benefit model for the general restriction of carnivorous plants to sunny, moist,
nutrient-poor habitats. American Naturalist 124: 479-497.

16. http://en.wikipedia.org/wiki/Carnivorous_plant

17. Hartmeyer, S. 1998. Carnivory in Byblis revisited II: the phenomenon of symbiosis on insect
trapping plants. Carnivorous Plant Newsletter 27(4): 110-113.

18. What is a carnivorous plant? http://www.omnisterra.com/botany/cp/html/cp_defin.htm

19. Miller, M. 2002. http://home.paonline.com/mrmiller/Names.HTM

20. Anderson, B. and J.J. Midgley. 2003. Digestive mutualism, an alternate pathway in plant
carnivory. Oikos. 102(1): 221-224.

21. Stern, K.R. 1988. Introductory Plant Biology. Fourth Edition. William C. Brown
Publishers. Dubuque, Iowa.

57
22. Hansen, E. 1999. Bee bop-reproduction of the bucket orchid.
http://www.findarticles.com/p/articles/mi_m1134/is_2_108/ai_54032991

23. http://www.imdb.com/title/tt0091419/

24. http://www.absoluteastronomy.com/encyclopedia/c/ca/carnivorous_plant.htm

25. Sutton, J. 1998. http://web.unbc.ca/~ackerman/biol402-prospectus.htm

26. Anderson, B. and J.J. Midgley. 2002. It takes two to tango but three is a tangle: mutualists
and cheaters on the carnivorous plant Roridula. Oecologia 132: 369-373.

27. Newell, S.J. and A.J. Nastase. 1998. Efficiency of insect capture by Sarracenia purpurea
(Sarraceniaceace), the northern pitcher plant. American Journal of Botany 85(1): 88-91.

28. Zamora, R., J.M. Gomez, J.A. Hodar. Responses of a carnivorous plant to prey and inorganic
nutrients in a Mediterranean environment. Oecologia 111(4): 443-451.

29. Lindzey, S. 2001. The biogeography of the California pitcher plant (Darlingtonia
californica). www.rook.org/earl/bwca/nature/aquatics/sarracenia.html

30. Zamora, R., J. M. Gomez, and J.A. Hodar. 1998. Fitness responses of a carnivorous plant in
contrasting ecological scenarios. Ecology 79(5): 1630-1644.

31. Miller, M. 2002. Basic growing instructions for all carnivorous plants
http://home.paonline.com/mrmiller/Basic.HTM

32. Murphy, P.B. and R.S. Boyd. 1999. Population status and habitat characterization of the
endangered plant, Sarracenia rubra subspecies alabamensis. Castanea 64(2): 101-113.

33. Barker, N.G. and G.B. Williamson. 1988. Effects of a winter fire on Sarracenia alata and S.
psittacina. American Journal of Botany 75(1): 138-143.

34. Rebertus, A.J., G.B. Williamson, and E.B. Moser. 1989. Longleaf pine pyrogenicity and
turkey oak mortality in Florida xeric sandhills. Ecology 70(1): 60-70.

35. Brewer, J.S. 1998. Effects of competition and litter on a carnivorous plant, Drosera
capillaris (Droseraceae). American Journal of Botany 85(11): 1592-1596.

36. Sutton, J. 1998. Reproductive strategy and prey capture frequency of the purple pitcher plant
(Sarracenia purpurea). http://web.unbc.ca/~ackerman/biol402-research-proposal.htm

37. Buckley, H.L., T.E. Miller, et al. 2003. Reverse latitudinal trends in species richness of
pitcher-plant food webs. Ecology Letters 6: 825-829.

38. Bradshaw, W.E. and R.A. Creelman. 1984. Mutualism between the carnivorous purple
pitcher plant and its inhabitants. American Midland Naturalist 112(2): 294-304.

39. Ellison, A.M. and N.J. Gotelli. 2002. Nitrogen availability alters the expression of carnivory
in the northern pitcher plant, Sarracenia purpurea. Proceedings of the National Academy of
Sciences 99(7): 4409-4412.

58
40. Thoren, L.M., J. Tuomi, et al. 2003. Resource availability affects investment in carnivory in
Drosera rotundifolia. New Phytologist 159: 507-511.

41. Zamora, R. 1999. Conditional outcomes of interactions: the pollinator-prey conflict of an

insectivorous plant. Ecology 80(3): 786-795.

42. Gibson, T.C. 1991. Competition among threadleaf sundews for limited insect resources.
The American Naturalist 138(3): 785-789.

43. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=1288
3887&dop=Abstract

44. Murza, G.L. and A.R. Davis. 2005. Flowering phenology and reproductive biology of
Drosera anglica (Droseraceae). Botanical Journal of the Linaean Society 147: 417-426.

45. Murza, G.L. and A.R. Davis. 2003. Comparative flower structure of three species of sundew
(Drosera anglica, Drosera linearis, and Drosera rotundifolia) in relation to breeding system.
Canadian Journal of Botany 81: 1129-1142.

46. Bronstein, J.L. 1994. Conditional outcomes in mutualistic interactions. Trends in Ecology
and Evolution 9(6): 214-217.

47. Slippery surfaces on carnivorous plants. http://www.botany.ubc.ca/people/jetter.htm

48. Joel, D.M., B.E. Juniper, and A. Dafni. 1985. Ultraviolet patterns in the traps of carnivorous
plants. New Phytologist 101: 585-596.

49. Cresswell, J.E. 1991. Capture rates and composition of insect prey of the pitcher plant
Sarracenia purpurea. The American Midland Naturalist 125(1): 1-9.

50. Gorb, E, V. Kastner, et al. 2004. Structure and properties of the glandular surface in the
digestive zone of the pitcher in the carnivorous plant Nepenthes ventrata and its role in insect
trapping and retention. The Journal of Experimental Biology 207: 2947-2963.

51. Merbach, M.A., D.J., Merbach, et al. 2002. Mass march of termites into the deadly trap.
Nature 415: 36-37.

52. Heard, S.B. 1994. Pitcher-plant midges and mosquitoes: a processing chain commensalism.
Ecology 75(6): 1647-1670.

53. Staff of the L.H. Bailey Hortorium, Cornell University. 1976. Hortus Third. Macmillan
Publishing Company. New York.

54. Curtis, H. and N.S. Barnes. 1989. Biology. Fifth Edition. Worth Publishers, Inc. New
York.

55. Radford, A.E., H.E. Ahles, and C.R. Bell. 1968. Manual of the Vascular Flora of the
Carolinas. University of North Carolina Press, Chapel Hill, N.C.

59
56. Lichtner, F.T. and S.E. Williams. 1977. Prey capture and factors controlling trap narrowing
in Dionaea (Droseraceae). American Journal of Botany 64(7): 881-886.

57. Daemon, D. 2005. Beauty in a bug eater: A lifetime fostering flytraps in their native habitat.
NC State Magazine. Spring. p. 55.

58. Moyle, Peter. 1995. Fish: An Enthusiasts Guide. The University of California Press.
Berkley, California.

59. Adamec, L. 1997. Mineral nutrition of carnivorous plants: a review. Botanical Review. 63:
273-299.

60. Gibson, T.C. 1991. Differential escape of insects from carnivorous plant traps. American
Midland Naturalist: 125(1): 55-62.

61. Cresswell, J.E. 1993. The morphological correlates of prey capture and resource parasitism
in pitchers of the carnivorous plant Sarracenia purpurea. The American Midland Naturalist
129(1): 35-41.

62. Fish, D. and D.W. Hall. 1978. Succession and stratification of aquatic insects inhabiting the
leaves of the insectivorous pitcher plant, Sarracenia purpurea. The American Midland
Naturalist 99(1): 172-183.

63. Anderson, B. and J.J. Midgley. 2001. Food or sex; pollinator-prey conflict in carnivorous
plants. Ecology Letters 4(6): 511-513.

64. Introduction to North American Carnivorous Plants Fact Sheet

http://hua.huh.harvard.edu/FNA/Outreach/FNA_fsintro_carnivory.shtml

65. Kaul, R.B. 1982. Floral and fruit morphology of Nepenthes lowii and N. villosa, montane
carnivores in Borneo. American Journal of Botany 69(5): 793-803.

66. Elder, C.L. 1994. Reproductive biology of Darlingtonia californica.

www.omnisterra.com/botany/cp/pictures/darlingt/0074.htm

67. Pollination. http://www.carnivorousplants.org/seedbank/species/Sarracenia.htm

68. Smith, R.L. 1990. Ecology and Field Biology. Fourth Edition. Harper and Row Publishers.
New York.

69. Wilson, P. 1994. The east-facing flowers of Drosera tracyi. The American Midland
Naturalist 131: 366-369.

70. Staton, M.L. and C. Galen. 1989. Consequences of flower heliotropism for reproduction in
an alpine buttercup (Ranunculus adoneus). Oecologia 78: 477-485.
71. Zhang, H., J.M. Pleasants, and T.W. Jurik. 1991. Development of leaf orientation in the
prairie compass plant, Silphium laciniatum L. Bulletin of the Torrey Botanical Club 118 (1):
33-42.

60
72. Anderson, B. J.J.Midgley, and B.A. Stewart. 2003. Facilitated selfing offers reproductive
assurance: a mutualism between a hemipteran and carnivorous plant. American Journal of
Botany 90(7): 1009-1015.

73. Clarke, C.M. and R.L. Kitching. 1995. Swimming ants and pitcher plants: a unique ant-
plant interaction from Borneo. Journal of Tropical Ecology 11: 589-602.

74. Cochran-Stafira, D.L. and C.N. von Ende. 1998. Integrating bacteria into food webs:
studies with Sarracenia purpurea inquilines. Ecology 79(3): 880-898.

75. Naeem, S. 1988. Resource heterogeneity fosters coexistence of a mite and a midge in pitcher
plants. Ecological Monographs 58(3): 215-227.

76. Miller, T., D. Cassill, et al. 1994. Intraspecific and interspecific competition of Wyeomyia
smithii (Coq.) (Culicidae) in pitcher plant communities. The American Midland Naturalist
131(1): 136-145.

77. Trzcinski, M.K., S.J. Walde, and P.D. Taylor. 2003. Colonisation of pitcher plant leaves at
several spatial scales. Ecological Entomology 28: 482-489.

78. Hartmeyer, S. 1998. Carnivory in Byblis liniflora revisited II: the phenomenon of symbiosis
on insect trapping plants. Carnivorous Plant Newsletter 27(4): 110-113.

79. Addicott, J.F. 1974. Predation and prey community structure: an experimental study of the
effect of mosquito larvae on the protozoan communities of pitcher plants. Ecology 55: 475-
492.

80. Nastase, A.J., C. De La Rosa, and S.J. Newell. 1995. Abundance of pitcher-plants
mosquitoes, Wyeomyia smithii (Coq.) (Diptera: Culicidae) and midges, Metriocnemus knabi
Coq. (Diptera: Chironomidae), in relation to pitcher characteristics of Sarracenia purpurea
L. The American Midland Naturalist 133(1): 44-51.

81. Bergland, A.O. M. Agotsch, et al. 2005. Factors influencing the seasonal life history of the
pitcher-plant mosquito, Wyeomyia smithii. Ecological Entomology 30: 129-137.

82. Rabenold, K.N. 1979. A reversed latitudinal diversity gradient in avian communities of
eastern deciduous forests. The American Naturalist 114: 275-286.

83. Keever, C. 1950. Causes of succession on old fields of the Piedmont, North Carolina.
Ecological Monographs 20: 231-250.

84. Schafale, M. and N.L. Christensen. 1986. Vegetational variation among old fields in
Piedmont North Carolina. Bulletin of the Torrey Botanical Club 113(4): 413-420.

85. Burrell, C.C. 2005. 10-gallon bog. Horticulture April. p. 24.

86. Anderson, B. 2004. Comparative population genetic structures and local adaptation of two
mutualists. Evolution 58(8): 1730-1748.

87. Perry, D.A. 1994. Forest Ecosystems. The Johns Hopkins University Press. Baltimore,
MD.

61
88. Sanders, I.R., R.T. Koide, and D.L. Shumway. 1997. The role of mycorrhizal symbiosis. In
Diversity and Structure in Natural Communities. Editor? Publisher? Pages?

89. Newman, E.I. and K. Ritz. 1986. Evidence on the pathway of phosphorus transfer between
vesicular-arbuscular mycorrhizal plants. New Phytologist 104: 77-87.

90. Brown, D.G. 2001. Indirect effects.

http://www.users.csbsju.edu/~dgbrown/BIOL338/indirect.html.

91. Takabayashi, J. and M. Dicke. 1996. Plant-carnivore mutualism through herbivore-induced

carnivore attractants. Trends in Plant Science 1(4): 109-113.

92. Schultz, J.C. and I.T. Baldwin. 1982. Oak leaf quality declines in response to defoliation by
gypsy moth larvae. Science 217(4055): 149-151.

93. Schultz, J.C. and I.T. Baldwin. 1983. Rapid changes in tree leaf chemistry induced by
damage: Evidence for communication between plants. Science 221(4607): 277-279.

94. Strauss, S. Y., and W. S. Armbruster. 1997. Linking herbivory and pollination - new
perspectives on plant and animal ecology and evolution. Ecology 78(6): 1617-1618.

95. McIntyre, J. The role of plants in attracting predators and parasitoids to control herbivore
feeding.
http://www.colostate.edu/Depts/Entomology/courses/en570/papers_1996/mcintyre.html

62