Literature Review

Part I: Carnivorous Plants

From the 1975 Masters Thesis: Bacteriological and ecological observations on the northern pitcher plant, Sarracenia purpurea. John A. Lindquist. Department of Bacteriology, University of Wisconsin, Madison, WI.

A. Introduction

The amount of literature on the subject of carnivorous plants is extensive, though far from comprehensive and up to date. This review of the literature, besides giving a general overview of carnivorous plants, will emphasize the pitcher plants, especially Sarracenia purpurea.

Carnivorous (also called insectivorous) plants possess modified leaves designed to trap and digest small animals, especially insects. The absorption of nutrients by this means supplements that of the roots, as carnivorous plants generally grow in nutrient-poor soil.

There are two basic trapping mechanisms. The Venus fly-trap, for example, "actively" moves to engulf insects in contact with it. In contrast, the pitcher plant serves as a "passive" pitfall for insects: no plant movements are ever involved. In either case, the entrapped insects are subsequently digested by enzymes produced by bacteria and/or the plant itself.

The occurrence of carnivorous plants in two groups of families of green plants indicates that the carnivorous habit arose at least twice in the plant kingdom (Lloyd, 1942). Some microscopic species of fungi also catch and digest animal prey by either snares (actively) or sticky discs (passively). Arthrobotrys oligosperma snares nematodes in loops of its hyphae, and specialized digesting and absorbing hyphae are then sent into the prey (Shetler, 1972).

If one may speculate as to evolution, carnivorous plants probably developed from non-carnivorous plants, possibly those finding poor soil unsuited for proper growth. In any of these ancestral species, a gradual evolution of the leaf structure, via surviving mutations, may have lead to a form which could passively entrap small invertebrates and absorb nitrogenous and mineral nutrients from their decay. This would have enabled the plant to supplement intake of nutrients from the roots. Further evolution would have proceeded in a number of directions, leading to refinements of various active and passive mechanisms of trapping animals as well as to the establishment of a general dependency for nutrient-poor substrates. In some more recently evolved forms, such as the Venus flytrap, plant enzymes have developed, supplementing or supplanting the action of bacteria in the digestive process.

Many carnivorous plants can be found in acidic environments. As has been shown with pitcher plants, there is no requirement for the acidity per se. Nutrients in acidic environments are characteristically low in availability, low enough not to encourage excess competition or cause damage to the plants which are unable to thrive in nutrient-rich substrates. Pitcher plants are occasionally found in neutral and alkaline areas which are otherwise nutrient-poor (Wherry, 1929; Mandossian, 1965).

Placing as his evidence the efficient attracting, trapping and digestive abilities of pitcher plants, Jones (1935) stated: "That the pitcher plants are 'intended' as insect traps – that their capture of insects is not an accident of evolution and of no real significance to the plants – is attested by a mass of evidence which in its entirety is overwhelming."

B. Taxonomy, Descriptions and Habitats

B1. The Genera of Carnivorous Plants

Classification of the green carnivorous plants, all of which are angiosperms (flowering plants) and dicotyledons (plants with two seed leaves), is based primarily on floral characteristics. Most of the species of carnivorous plants belong to the family Lentibulariaceae which have bilaterally symmetrical flowers with fused petals. The remaining species belong to various families having radially-symmetrical flowers with separate petals (Shetler, 1972).

Table 1 lists the genera of carnivorous plants together with general information on their taxonomy, trapping mechanisms and ranges.

B2. Sarracenia purpurea – Taxonomy

Of the species of North American pitcher plants (the genera Sarracenia and Darlingtonia), Sarracenia purpurea is the one most widespread and is the type example of a pitcher plant in morphology and carnivorous habit. It is also the type species of its genus. S. purpurea, sometimes called the "sidesaddle pitcher plant" (Wherry, 1929), exists as two subspecies. S. purpurea purpurea (formerly ssp. gibbosa), the "northern pitcher plant", is found from Maine to Delaware, westward through Minnesota and over a vast area in Canada. A mutant lacking the anthocyanin pigments and thus having yellow instead of red flowers, once known as S. heterophylla, is now considered "forma heterophylla" of the northern subspecies (Wherry, 1929; Schnell, 1974). Another possible form of this subspecies, "S. purpurea stolonifera", was described in the 1930's as having especially elongated rhizomes (Walcott, 1935). S. purpurea venosa, the "southern pitcher plant", is found from New Jersey through the southeastern states (Wherry, 1935; Schnell, 1974).

B3. Sarracenia purpurea – Habitats

Sarracenia purpurea is generally found in acidic swamps, bogs and wet meadows over its range. The northern subspecies inhabits, though is not restricted to, the bogs of the northern forested regions of North America.

Bogs are formed in depressions left by the last ice sheet which accumulate water and are poorly drained. Eventually the depressions are invaded by floating mats of vegetation. As the water movement becomes reduced and the usually dominant moss, Sphagnum, renders the water acidic, an acidic, anaerobic environment develops, slowing down the decomposition of the accumulating organic matter. The coldness of the water, due to cooling by evaporation and little absorption of sun heat, also retards decomposition (Calef, 1971; Smith, 1966).

The slowly-decomposing organic deposit, which eventually becomes "peat," consists almost entirely or organic materials with a very small amount of minerals. The nutrient elements nitrogen, potassium and phosphorus are tied up in the peat and are available in very limited amounts to the vegetation. When the sphagnum mat becomes strong enough to support considerable weight, a variety of plants (including carnivorous plants such as Sarracenia and Drosera) find this a favorable environment for one or more reasons, e.g. low available nutrients, high acidity, limited competition and high moisture (Smith, 1966; Calef, 1971). A study by Wherry (1929) of about fifty wetland habitats of S. purpurea was made with regard to the substrate pH. With indicator dyes, a "mediacid" (pH 4.1 – 5.0) reaction was usually found; the overall range was from "superacid" (pH 3.1 – 4.0) to "minimalkaline" (pH 7.1 – 7.9). Total nitrogen determinations on the soils of acid and neutral bogs in New York revealed between 2 and 3 per cent nitrogen, but no nitrate or ammonia could be detected.

Five bogs in Michigan were tested with a pH meter by Mandossian (1965). At the root level of S. purpurea, the reactions ranged from 5.2 to 8.9. The acidic reactions were associated with the presence of sphagnum moss which was not present in the alkaline bogs. Also, no obligate association of S. purpurea with another plant or group of plants was noted.

According to Lloyd (1942), mycorrhizal fungi are not generally associated with the roots of carnivorous plants. However, Shreve (1906) noted fungal threads covering and penetrating the root epidermis of cultivated seedlings of S. purpurea grown in highly saturated sphagnum moss.

B4. Sarracenia purpurea – Morphology and Development of the Leaf

The generalized structure of a fully-developed, opened leaf on a mature plant is shown in Figure 1. The orifice, bounded by the hood and the "nectar roll", easily admits rain into the pitcher cavity and also insects which drown and decompose in the water. Little if any liquid is produced by the plants. The beads of moisture often observed in young leaves which have not yet collected rain probably originate from dew.

Various early botanists regarded the pitcher as being formed by the fusion of the edges of the leaf blade. Others believed the tube to be a hollow petiole with the hood representing the leaf blade. Both views have persisted in the literature through the present time. However, modern research on the morphogenesis of the pitcher leaf has shown that the cavity arises simply as a consequence of the gradual lengthening of the margins of a hollow blade, the petiole being very short. The rigidity of the pitcher is assisted by the wing (Lloyd, 1942).

If S. purpurea is grown under low light intensity such as in constant shade or artificially in a poorly-illuminated room, new leaves are flat and blade-like, each leaf being composed of a very narrow pitcher cavity and a grossly enlarged wing (Lloyd, 1942; Mandossian, 1966a).

The orifice is not open during the early development of the leaf. The edges of the hood form a seal over the cavity, parting before the leaf attains its maximum size. In the fully developed leaf, the hood flares outward, and the nectar roll assumes its mature form.

The leaves of the tiny seedling plants, called "juvenile" leaves, are strikingly different in appearance from the leaves of the mature plants, In the open juvenile leaves, the hood arches over the orifice, rendering it lateral rather than terminal to the main leaf axis, somewhat like the mature leaf of S. psitticina. The nectar roll is undeveloped, and the cavity is relatively long and slender (Lloyd, 1942).

The growth of a single plant from seedling to the mature, blooming form may take five or six years. During this time, the leaves, which arise throughout the growing season, may be found in juvenile, intermediate or mature form depending on the age of the plant (Shreve, 1906).

The leaves form a rosette above the central axis of the plant. As the new leaves arise each warm season, they are erect, and as they develop they tend to become more lateral. As the older leaves fill with rain and insects and the newer leaves arise at a higher level on the rosette, the older leaves become characteristically "decumbent," a key feature distinguishing this species from most of the other species of Sarracenia (Wherry, 1935). Eventually the old leaves become crowded into the substratum and slowly decompose, adding to the nutrient pool of the substrate (Plummer, 1963).

B5. Sarracenia purpurea – Differential Morphology of the Leaf

The northern and southern subspecies of Sarracenia purpurea are differentiated by the relative length and width of the leaves, the hairiness of the outer surface of the pitchers and the species of commensal mosquito larvae (discussed later), as well as by their respective habitat ranges. Intermediate forms are found where the ranges overlap. S. purpurea purpurea has relatively long and slender leaves which are smooth and slippery to the touch; S. purpurea venosa has relatively short and wide leaves which are covered with hairs and feel rough (Wherry, 1935; Wherry, 1973b). The outer leaf surface in both subspecies is studded with numerous nectar glands which lure insects to the leaves (Lloyd, 1942).

The inner leaf surface of S. purpurea is visibly divided into the zones numbered in Figure 1. Comparable zones can be found in some other species of Sarracenia. Zone 1, the "attractive" zone, comprises the "inner" surface of the hood; the epidermis supports stomata, nectar glands and strong, downwardly-slanting hairs which probably assist in directing insects into the pitcher cavity. Zone 2 is the narrow "conducting" zone, consisting of glassy cells, overlapping like tiles on a roof, affording no foothold for insects attempting to crawl up. No hairs or stomata are present, but there are numerous nectar glands, making this zone also "attractive" (Lloyd, 1942; Hooker, 1874).

Zone 3, the "glandular" zone, generally occupies most of the internal cavity. This smooth, polished-appearing area is devoid of hairs and stomata, and numerous glands of questionable function appear among the heavily cutinized cells. Crawling insects find this zone difficult if not impossible to climb. Yet they may be able to crawl over the nectar roll if the pitcher is entirely filled with rain (Lloyd, 1942; Hooker, 1874).

Zone 4, the "detentive" zone, which is also considered an absorptive area, is devoid of cuticle except about the downwardly-pointing hairs. No glands or stomata are present. When little or no water is present in the pitcher, the hairs serve to wedge any struggling insect toward the lower part of the cavity. The relative lack or cuticle assists in the absorption of materials which can be demonstrated with dyes such as methylene blue (Lloyd, 1942; Hooker, 1874).

Zone 5, which apparently has no special function, has a continuous cuticle and is hairless in the lower area. Methylene blue enters the cells of this zone much more easily than the cells of zone 3 but less easily than those of zone 4. No glands or stomata are present. As will be indicated later concerning the digestive and absorptive properties of pitcher plants, Sarracenia flava possesses a lengthened lower zone, considered "absorptive" and somewhat analogous to zone 5 of S. purpurea (Lloyd, 1942).

These zones are also present in the juvenile leaf. However, zone 3 is a narrow area; the bulk of the cavity wall consists of the hairy zone 4 (Lloyd, 1942).

B6. Sarracenia purpurea – Studies on Acidity of the Pitcher Fluid

Observations on acidity were made over a four-month period (May – August) on Sarracenia purpurea pitcher fluid by Higley (1835), probably in Wisconsin. These tests were made on pitchers arising during that season and then collected for analysis. The acidity of the pitcher fluid became greater each month, as did the accumulation of insect remains. It was especially high in July and August, when malic and citric acids were identified. The former acid predominated and was believed to have been drawn from the leaf tissue into the fluid and to serve as an aid to digestion.

An extensive survey by Wherry (1929) of pH readings of the pitcher fluid showed a "mediacid" average (pH 4.1 – 5.0) and a range from "superacid" (pH 3.1 – 4.0) to "subalkaline" (pH 8.0 -8.9), varying about as much as the pH of the bog but showing no correlation. No one locality was studied over any length of time, nor were the ages of the leaves indicated. Pitcher leaves on the same plant often varied widely in their pH. Rain was believed to account for a part of the acidity, and the alkalinity of some pitchers was attributed to the decay of insects, releasing ammonia. In some cases high acidity was attributed to the entrapment of formic acid-secreting ants.

In New Jersey a number of S. purpurea pitchers of various ages were examined for pH by Hepburn and Jones (1927b) with Wherry's colorimetric method. A slight alkaline reaction was prevalent in the fluid of newly-opened pitchers, and the reaction was more frequently acid in the fluid of older pitchers.

Results of tests by Swales (1969) in Quebec in September showed a pH range of 4.1 to 4.6 for older S. purpurea pitchers "with the flaps up and a fair amount of fluid" and a range of 7.0 to 7.3 for younger leaves "with the flaps down and little fluid within." Accumulation of carbon dioxide from the atmosphere and the byproducts of insect degredation were cited as probable reasons for the acidity.

As a result of these observations on S. purpurea, a general correlation was seen between acidity, advancing age of the leaf and accumulation of insect remains. The exact causes of acidity and its increase constitute a wide-open field for investigation. The following explanations, offered in part by the previously-cited investigations, are possible:

Changes in pH during digestion have been studied for other Sarracenia species. In a bacteriological study of S. flava, Plummer and Jackson (1963) showed that digestion of insects (except ants) produced an alkaline pH due to ammonifying bacteria. No return to a post-digestion, lower-pH condition was noted nor looked for, however, the ability of the plant to act as a buffering influence was suspected. Earlier studies by Jones and Hepburn (1927) on several pitcher plant species showed a return to the normal pitcher fluid reaction within a few days after the introduction of dilute acidic or alkaline solutions.

B7. Sarracenia purpurea – Morphology of the Flower

The peculiar flower structure of S. purpurea and its means of pollination are shared with the other species of the genus. It was often noted that mature S. purpurea plants do not flower every year. However, this may be attributed to late spring frosts, once seen to completely destroy all buds in a locality (Mandossian, 1966b). As the bud develops in a normal spring, the stalk near the bud bends; when the petals expand, the flower opens downward. The flower is perfect, with 70 to 80 stamens and a style which is expanded into an inverted, umbrella-shaped structure. The stigmata appear at the five points of the umbrella which protrude between the five inverted petals (Jones, 1935; Shreve, 1906). Pollen falls into the concavity of the style, and insects are apparently needed to move pollen from the floor of the style to the stigmatic points of the same or a different flower (Jones, 1935). Cross-pollination is considered necessary for good seeds. Various species of Sarracenia growing in the same locality very readily cross-pollinate and form viable hybrids if their flowers develop at about the same time (Macfarlane, 1917). A period of seed dormancy is necessary for an optimum germination rate; this dormancy is satisfied by over-wintering (Mandossian, 1966b).

B8. Other Species of Sarracenia

The seven species of Sarracenia other than S. purpurea are listed below with the common names associated with them in the literature (Wherry, 1935; Wherry, 1973b; Schnell, 1974):

S. oreophilagreen pitcher plant
S. alata (S. sledgei)pale pitcher plant
S. flavayellow pitcher plant
S. leucophylla (S. drummondii)whitetop pitcher plant
S. rubrasweet pitcher plant
S. rubra jonesii (S. jonesii)red pitcher plant
S. minor (S. variolaris, S. adunca)hooded pitcher plant
S. psitticinaparrot pitcher plant

Many horticultural "varieties" and "species" are known, but they actually represent forms and hybrids, occasionally observed in nature.

Compared to S. purpurea, the leaves of these species are long and narrow; S. leucophylla leaves attain a length of three feet. The orifice is not closely covered by the hood in these species except for S. minor and S. psitticina which have small orifices opening laterally to the leaf axis and nearly closed off by the hood. The mature leaves of S. psitticina are usually in a decumbent position. The leaves of the other species are generally erect. Depending on the species, the flowers are yellow or red (Walcott, 1935). The gap between flower and leaf production during the growing season is generally marked for S. flava, S. leucophylla and S. psitticina (Argo, 1964).

These seven species are found in overlapping ranges in the Atlantic and gulf coastal plain from Texas to Virginia and into the highlands of the southeastern states. The habitats are generally acid swamps, moist meadows and pinelands. S. oreophila, however, is peculiar in its preference for the acidic sands and gravels of stream banks. S. psitticina may be considered semi-aquatic; the decumbent leaves often fill with swamp water (Wherry, 1935).

In many localities, pitcher plants of all species are being threatened, as land development for farming and recreation and careless over-collecting proceed uncontrolled. It has been recently lamented that the red pitcher plant, S. rubra jonesii (S. jonesii) is being rapidly exterminated from its natural habitat. Wherry (1973a) revisited the "type meadow" and found it had been converted into a potato field; most of the other localities of this rare plant have also gone under. Extinction of this subspecies causes little concern for the taxonomic "lumpers" who do not accord the plant any special status, not even subspecies. Most (perhaps all) S. jonesii plants survive only under artificial cultivation, a situation which may be reasonably expected in the future for other species of Sarracenia.

The pH ranges of the habitats and open-pitcher fluid were determined by Wherry (1929) for the non-S. purpurea species (except S. oreophila). The habitats were usually "mediacid" (pH 4.1 – 5.0) except for S. rubra jonesii which was usually "subacid" (pH 5.1 – 6.0). No variation was seen as extreme as that for S. purpurea. An average "mediacid" pitcher fluid reaction was also generally found except for S. alata and S. leucophylla which were most often neutral. S. alata and S. leucophylla pitchers were suspected of secreting neutral or alkaline substances; the pH readings, ranging from "subacid" to slightly alkaline, varied more than those of the other species except S. purpurea.

As is reported for S. purpurea, the secretion of fluid by the plant into the pitcher cavity is virtually nil for S. psitticina; pitchers of other species produce easily measurable amounts. A study of pitcher fluid from closed pitchers (before contamination by bacteria, insects, etc.) was made by Jones and Hepburn (1927). With red and blue litmus paper, acidic reactions were noted for S. alata, S. flava, S. leucophylla (marked) and S. rubra (slight). A neutral reaction was noted for S. minor. The pH of fluid from "new" laboratory-grown pitchers of S. flava was determined by Plummer and Jackson (1963) to average 4.5; without insect feeding, an average of 6.2 was attained in 22 days with an increase in fluid.

C. Evolution of Sarracenia Species

A comparative study of the morphology, habitats and probable history of migrations can give an indication of the possible evolutionary relatedness of the species of Sarracenia. Most of the territory between the rail line, which marked the boundary of the Atlantic Ocean prior to and during the Cretaceous, and the southern limit of the Wisconsin ice sheet has been continuously open for occupancy since Cretaceous times, which marked the appearance of plants with modern aspects. The "primitive" species S. oreophila, the presumed ancestor of the other species of the genus, is believed to have remained in its original home, the Appalachian Mountains region of northeastern Alabama (Wherry, 1935).

When the Appalachian region uplifted during the Tertiary with the retreat of the ocean, exposing the present Atlantic coastal plain, Sarracenia (and other plants) migrated according to temperature and substrate requirements and adapted to conditions formerly hostile via surviving mutations. The northernmost species, S. purpurea, migrated to what is now New Jersey. With the retreat of the Wisconsin ice sheet, leaving the northern bogs, the morphologically different and supposedly highly aggressive variant of the species, S. purpurea purpurea , migrated into the "glacial" area (Wherry, 1935).

D. Animal Associates of Sarracenia purpurea

D1. Entrapments

From studies of the contents of S. purpurea pitchers in Quebec, Swales (1972) found a variety of insect and nematode entrapments. Twenty-nine families of the following insect orders were found: Orthoptera, Hemiptera, Coleoptera, Lepidoptera, Diptera and Hymenoptera. Among the nematodes collected were two specimens or a grasshopper parasite, Agamomermis, which, when uncoiled, were found to attain lengths of 15.5 and 17.7 cm.

Small vertebrates are also entrapped in pitcher plants as indicated by Jones' (1935) study of the large southern species in which he round bones of small green tree toads and chameleon lizards. These animals often sit near the pitcher orifices and consume insects attracted to the plants.

D2. Commensals

Several groups of invertebrates live in the fluid of the pitcher cavity and are not digested. Besides the often-noted larvae of mosquitoes (Wyeomyia smithii), gnats (Metriocnemus knabi) and sarcophagid flies (Blaesoxipha fletcheri), Swales (1972) found living rotifers, nematodes, mites and copepods. Two-thirds of the mosquito and gnat larvae were observed by Swales to survive an overwintering period in the frozen pitcher fluid, however, all sarcophagid fly larvae died. A similar study by Paterson (1971), also in Canada, showed the overwintering mortality of the mosquito and gnat larvae to be less than five per cent.

Wyeomyia larvae have been long known to obligately inhabit the fluid of Sarracenia purpurea. Wherry (1972) observed that the northern subspecies of S. purpurea is host to W. smithii, and the southern subspecies is host to W. haynei.

Several species of sarcophagid flies were seen by Jones (1935) to participate in the pollination of the flower. (Jones applied "sarcophagus" to the pitcher cavity.) Argo (1964) noted that each female fly deposits upward of a dozen living larvae per pitcher. The larvae are believed to cannibalize each other until one remains in the pitcher and develops to maturity.

The commensal larvae are aquatic in nature as opposed to the terrestrial entrapments which drown in the pitcher fluid. The production of antienzymes by the larvae has been suspected, as inhibitors to pepsin and trypsin have been recovered from the remotely analogous intestinal roundworm, Ascaris lumbricoides. No positive proof of inhibitors to the pitcher enzymes has been observed in any of the commensal invertebrates of pitcher plants (Swales, 1969; Lloyd, 1942).

D3. Parasites

A paper wasp has been observed nesting in pitchers in Massachusetts (Berman, 1969). Three species of parasitic moths have been observed on pitcher plants in Maine: one feeding on the leaves, one tunnelling into the rhizomes and one parasitizing the seed capsule (Brower and Brower, 1970). Adults of the moth Exyra rolandiana, closely associated with S. purpurea throughout its range, lay their eggs on the inner walls of the pitchers. The larvae close off the pitcher orifice with a thick net and feed on the inner layers of the pitcher wall. As with the sarcophagid flies, only one larva remains in each parasitized pitcher, overwintering in its larval form (Jones, 1935).

Go on to Part II of the Literature Review.
Go to the References.
Return to the Pitcher Plant Project "Index" Page.

Page last modified on 1/9/98 at 9:45 AM, CST.
John Lindquist, Department of Bacteriology, University of Wisconsin – Madison