A protocarnivorous plant (sometimes also paracarnivorous, subcarnivorous, or borderline carnivore), according to some definitions, traps and kills

insect Insects (from Latin ') are pancrustacean hexapod invertebrates of the class Insecta. They are the largest group within the arthropod phylum. Insects have a chitinous exoskeleton, a three-part body ( head, thorax and abdomen), three pa ...

s or other

animal Animals are multicellular, eukaryotic organisms in the biological kingdom Animalia. With few exceptions, animals consume organic material, breathe oxygen, are able to move, can reproduce sexually, and go through an ontogenetic stage ...

s but lacks the ability to either directly

digest Digest may refer to: Biology *Digestion of food *Restriction digest Literature and publications *'' The Digest'', formerly the English and Empire Digest *Digest size magazine format * ''Digest'' (Roman law), also known as ''Pandects'', a digest ...

or absorb nutrients from its prey like a

carnivorous plant Carnivorous plants are plants that derive some or most of their nutrients from trapping and consuming animals or protozoans, typically insects and other arthropods. Carnivorous plants still generate some of their energy from photosynthesis ...

. The morphological

adaptation In biology, adaptation has three related meanings. Firstly, it is the dynamic evolutionary process of natural selection that fits organisms to their environment, enhancing their evolutionary fitness. Secondly, it is a state reached by the po ...

s such as sticky

trichome Trichomes (); ) are fine outgrowths or appendages on plants, algae, lichens, and certain protists. They are of diverse structure and function. Examples are hairs, glandular hairs, scales, and papillae. A covering of any kind of hair on a p ...

s or pitfall traps of protocarnivorous plants parallel the trap structures of confirmed

s. Some authors prefer the term "protocarnivorous" because it implies that these plants are on the

evolution Evolution is change in the heritable characteristics of biological populations over successive generations. These characteristics are the expressions of genes, which are passed on from parent to offspring during reproduction. Variation ...

ary path to true carnivory, whereas others oppose the term for the same reason. The same problem arises with "subcarnivorous". Donald Schnell, author of the book ''Carnivorous Plants of the United States and Canada'', prefers the term "paracarnivorous" for a less rigid definition of carnivory that can include many of the possible carnivorous plants.Schnell, 2002 The demarcation between carnivorous and protocarnivorous is blurred by the lack of a strict definition of

botanical Botany, also called , plant biology or phytology, is the science of plant life and a branch of biology. A botanist, plant scientist or phytologist is a scientist who specialises in this field. The term "botany" comes from the Ancient Greek w ...

carnivory and

ambiguous Ambiguity is the type of meaning in which a phrase, statement or resolution is not explicitly defined, making several interpretations plausible. A common aspect of ambiguity is uncertainty. It is thus an attribute of any idea or statement ...

academic literature on the subject. Many examples of protocarnivorous plants exist, some of which are counted among the ranks of true carnivorous plants as a matter of historical preference. Further research into these plants' carnivorous adaptations may reveal that a few protocarnivorous plants do meet the more rigid definition of a carnivorous plant.

Historical observations

Historical observations of the carnivorous syndrome in plant species have been restricted to the more obvious examples of carnivory, such as the active trapping mechanisms of '' Drosera'' (the sundews) and '' Dionaea'' (Venus flytrap), though authors have often noted speculation about other species that may not be so obviously carnivorous. In one of the earlier publications on carnivorous plants,

Charles Darwin Charles Robert Darwin ( ; 12 February 1809 – 19 April 1882) was an English naturalist, geologist, and biologist, widely known for his contributions to evolutionary biology. His proposition that all species of life have descended ...

had suggested many plants that have developed adhesive glands, such as ''

Erica tetralix ''Erica tetralix'', the cross-leaved heath, is a species of flowering plant in the family Ericaceae, native to western Europe, from southern Portugal to central Norway, as well as a number of boggy regions further from the coast in Central Eur ...

'', '' Mirabilis longifolia'', ''

Pelargonium zonale ''Pelargonium zonale'' is a species of ''Pelargonium'' native to southern Africa in the western regions of the Cape Provinces, in the geranium family. It is one of the parents of the widely cultivated plant ''Pelargonium'' × ''hortorum'', ofte ...

'', '' Primula sinesis'', and '' Saxifraga umbrosa'', may indeed be carnivorous but little research has been done on them. Darwin himself only mentioned these species in passing and did not follow through with any investigation.Darwin, 1875 Adding to the small but growing list, Francis Lloyd provided his own list of species suspected of carnivory in his 1942 book on carnivorous plants, though these species and their potential were only mentioned in the introduction.Lloyd, 1942 Later, in a 1981 review of the literature, Paul Simons rediscovered Italian journal articles from the early 1900s that identified several additional sticky species that digested insect prey. Simons was surprised to find these articles lacking in the literature cited sections of many modern books and articles on carnivorous plants, suggesting that academic research has treated Lloyd's 1942 book as the authoritative and comprehensive source on pre-1942 research on the carnivorous syndrome.Simons, 1981

Defining carnivory

Debate about what criteria a plant must meet to be considered carnivorous has yielded two proposed definitions: one with strict requirements and the other less restrictive. Darlingtonia californica ne1

The strict definition requires that a plant must possess morphological adaptations that attract prey through scent or visual cues, capture and retain prey (e.g., the waxy scales of ''

Brocchinia reducta ''Brocchinia reducta'' is one of a few carnivorous plant, carnivorous Bromeliaceae, bromeliads. It is native to southern Venezuela, Brazil, Colombia, and Guyana, and is found in nutrient-poor soil. ''B. reducta'' adapts to different environments ...

'' or downward facing hairs of '' Heliamphora'' prevent escape), digest the dead prey through enzymes produced by the plant, and absorb the products of digestion through specialized structures. The presence of commensals is also listed as strong evidence of a long evolutionary history of carnivory. By this definition, many sun pitcher plants (''Heliamphora'')Field studies of '' Heliamphora'' have determined that some species ('' H. nutans'', '' H. heterodoxa'', '' H. minor'', and '' H. ionasi'') do not produce their own digestive enzymes (Jaffe ''et al.'', 1992). and the cobra lily (''Darlingtonia californica'')Hepburn ''et al.'' (1927) is referenced in Ellison and Farnsworth (2005) as the authoritative source on ''Darlingtonia'''s apparent lack of proteolytic enzymes. Ellison and Farnsworth (2005) also notes that ''Darlingtonia'' instead relies on "a

food web A food web is the natural interconnection of food chains and a graphical representation of what-eats-what in an ecological community. Another name for food web is consumer-resource system. Ecologists can broadly lump all life forms into one o ...

of bacteria, protozoa, mites, and fly larvae" to break down captured prey (Naeem, 1988; Nielsen, 1990). would not be included on a roster of carnivorous plants because they rely on

symbiotic Symbiosis (from Greek , , "living together", from , , "together", and , bíōsis, "living") is any type of a close and long-term biological interaction between two different biological organisms, be it mutualistic, commensalistic, or para ...

bacteria Bacteria (; singular: bacterium) are ubiquitous, mostly free-living organisms often consisting of one biological cell. They constitute a large domain of prokaryotic microorganisms. Typically a few micrometres in length, bacteria were am ...

and other organisms to produce the necessary

proteolytic Proteolysis is the breakdown of proteins into smaller polypeptides or amino acids. Uncatalysed, the hydrolysis of peptide bonds is extremely slow, taking hundreds of years. Proteolysis is typically catalysed by cellular enzymes called prote ...

enzymes. The broader definition differs mainly in including plants that do not produce their own digestive enzymes but rely on internal food webs or microbes to digest prey, such as '' Darlingtonia'' and some species of '' Heliamphora''. The original definition of botanical carnivory, set out in Givnish ''et al.'' (1984), required a plant to exhibit an adaptation of some trait specifically for the attraction, capture, or digestion of prey while gaining a fitness advantage through the absorption of nutrients derived from said prey. Upon further analysis of genera currently considered carnivorous, botanists widened the original definition to include species that use mutualistic interactions for digestion. Both the strict and broad definitions require absorption of the digested nutrients. The plant must receive some benefit from the carnivorous syndrome; that is, the plant must display some increase in fitness because of the nutrients obtained from its carnivorous adaptations. Increased fitness might mean improved growth rate, increased chance of survival, higher pollen production or seed set.

Degrees of carnivory

One prevailing idea is that carnivory in plants is not a black and white duality, but rather a spectrum from strict non-carnivorous

photoautotrophs Photoautotrophs are organisms that use light energy and inorganic carbon to produce organic materials. Eukaryotic photoautotrophs absorb energy through the chlorophyll molecules in their chloroplasts while prokaryotic photoautotrophs use chlorophyll ...

rose A rose is either a woody perennial flowering plant of the genus ''Rosa'' (), in the family Rosaceae (), or the flower it bears. There are over three hundred species and tens of thousands of cultivars. They form a group of plants that can be ...

, for example) to fully carnivorous plants with active trapping mechanisms like those of '' Dionaea'' or ''

Aldrovanda ''Aldrovanda'' is a genus of carnivorous plants encompassing one extant species (''Aldrovanda vesiculosa'', the waterwheel plant) and numerous extinct taxa. The genus is named in honor of the Italian naturalist Ulisse Aldrovandi, the founder of ...

''. However, passive traps are still considered fully carnivorous. Plants that fall between the definitions in the strict carnivorous/non-carnivorous demarcation can be defined as being protocarnivorous. It is thought that these plants that have evolved protocarnivorous habits typically reside in habitats where there is a significant nutrient deficiency, but not the severe deficiency in

nitrogen Nitrogen is the chemical element with the symbol N and atomic number 7. Nitrogen is a nonmetal and the lightest member of group 15 of the periodic table, often called the pnictogens. It is a common element in the universe, estimated at se ...

and

phosphorus Phosphorus is a chemical element with the symbol P and atomic number 15. Elemental phosphorus exists in two major forms, white phosphorus and red phosphorus, but because it is highly reactive, phosphorus is never found as a free element on Ea ...

seen where true carnivorous plants grow. The function of the protocarnivorous habit, however, need not be directly related to lack of nutrient access. Some classic protocarnivorous plants represent

convergent evolution Convergent evolution is the independent evolution of similar features in species of different periods or epochs in time. Convergent evolution creates analogous structures that have similar form or function but were not present in the last com ...

in form but not necessarily in function. ''

Plumbago ''Plumbago'' is a genus of 10–20 species of flowering plants in the family Plumbaginaceae, native to warm temperate to tropical regions of the world. Common names include plumbago and leadwort (names which are also shared by the genus ''Cerato ...

'', for example, possesses glandular trichomes on its calyces that structurally resemble the

tentacle In zoology, a tentacle is a flexible, mobile, and elongated organ present in some species of animals, most of them invertebrates. In animal anatomy, tentacles usually occur in one or more pairs. Anatomically, the tentacles of animals work main ...

s of '' Drosera'' and ''

Drosophyllum ''Drosophyllum'' ( , rarely ) is a genus of carnivorous plants containing the single species ''Drosophyllum lusitanicum'', commonly known as Portuguese sundew or dewy pine. In appearance, it is similar to the related genus '' Drosera'' (the sun ...

''.Schlauer, 1997 The function of the ''Plumbago'' tentacles is, however, disputed. Some contend that their function is to aid in

pollination Pollination is the transfer of pollen from an Stamen, anther of a plant to the stigma (botany), stigma of a plant, later enabling fertilisation and the production of seeds, most often by an animal or by Anemophily, wind. Pollinating agents can ...

, adhering seeds to visiting pollinators.Fahn and Werker, 1972 Others note that on some species (''

Plumbago auriculata ''Plumbago auriculata'', the cape leadwort, blue plumbago or Cape plumbago, is a species of flowering plant in the family Plumbaginaceae, native to South Africa."Botanica. The Illustrated AZ of over 10000 garden plants and how to cultivate them" ...

''), small, crawling insects have been trapped in the ''Plumbago'''s mucilage, which supports the conclusion that these tentacles could have evolved to exclude crawling insects and favor flying pollinators for greater seed dispersal or perhaps for protection against crawling insect predators.

Trapping mechanisms

There are visible parallels between the trapping mechanisms of carnivorous plants and protocarnivorous plants. ''

'' and other species with glandular trichomes resemble the flypaper traps of ''Drosera'' and ''Drosophyllum''. The pitfall traps of protocarnivorous plants, such as some ''Heliamphora'' species and ''Darlingtonia californica'', are so similar to those of true carnivorous plants that the only reason they may be considered protocarnivorous instead of carnivorous is that they do not produce their own digestive enzymes. There are also protocarnivorous

bromeliad The Bromeliaceae (the bromeliads) are a family of monocot flowering plants of about 80 genera and 3700 known species, native mainly to the tropical Americas, with several species found in the American subtropics and one in tropical west Africa, ...

s that form a pitfall trap in an "urn" of rosetted leaves that are held together tightly. There are also other plants that produce a sticky mucilage not necessarily associated with a tentacle or glandular trichome, but instead can be described more like a slime capable of trapping and killing insects.

Flypaper traps

Dr. George Spomer of the

University of Idaho The University of Idaho (U of I, or UIdaho) is a public land-grant research university in Moscow, Idaho. It is the state's land-grant and primary research university,, and the lead university in the Idaho Space Grant Consortium. The Universit ...

has discovered protocarnivorous activity and function in several glandular plant species, including ''

Cerastium arvense ''Cerastium arvense'' is a species of flowering plant in the pink family known by the common names field mouse-ear and field chickweed. It is a widespread species, occurring throughout Europe and North America, as well as parts of South America. ...

'', ''

Ipomopsis aggregata ''Ipomopsis aggregata'' is a species of biennial flowering plant in the phlox family (Polemoniaceae), commonly known as scarlet trumpet, scarlet gilia, or skyrocket because of its scarlet red flowers with lobes curving back as if blown back by r ...

'', ''

Heuchera cylindrica ''Heuchera cylindrica'' is a species of perennial flowering plant in the Saxifragaceae, saxifrage family known by the common names poker alumroot, roundleaf alumroot, and coral bells. It is native to western North America, where it is found from ...

'', '' Mimulus lewisii'', '' Penstemon attenuata'', '' Penstemon diphyllus'', '' Potentilla glandulosa'' var. ''intermedia'', '' Ribes cereum'', ''

Rosa nutkana ''Rosa nutkana'', the Nootka rose, bristly rose, or wild rose is a perennial shrub in the rose family (Rosaceae).Rosa woodsii'' var. ''ultramontana'', ''

Solanum tuberosum The potato is a starchy food, a tuber of the plant ''Solanum tuberosum'' and is a root vegetable native to the Americas. The plant is a perennial in the nightshade family Solanaceae. Wild potato species can be found from the southern United ...

'', ''

Stellaria americana ''Stellaria'' is a genus of about 190 species of flowering plants in the family Caryophyllaceae, with a cosmopolitan distribution. Common names include starwort, stitchwort and chickweed. Description ''Stellaria'' species are relatively small ...

'', and '' Stellaria jamesiana''. These species tested positive for

protease A protease (also called a peptidase, proteinase, or proteolytic enzyme) is an enzyme that catalyzes (increases reaction rate or "speeds up") proteolysis, breaking down proteins into smaller polypeptides or single amino acids, and spurring the ...

activity, though it is unclear whether the protease is produced by the plant or by surface microbes. Two other species evaluated by Dr. Spomer, ''

Geranium viscosissimum ''Geranium viscosissimum'', commonly known as the sticky purple geranium, is a perennial in the flowering plant family Geraniaceae. It is thought to be a protocarnivorous plant. Distribution This herbaceous perennial plant is native to the Nort ...

'' and ''

Potentilla arguta ''Drymocallis arguta'', commonly known as the tall cinquefoil, prairie cinquefoil, or sticky cinquefoil, is a perennial herbaceous plant native to North America. It was formerly included with the typical cinquefoils in the genus '' Potentilla''. ...

'', exhibited protease activity and were further examined with ¹⁴C-labeled algal protein for nutrient absorption activity. Both of these latter species displayed an ability to digest and absorb the labeled protein. Other plants that are considered to be protocarnivorous have sticky trichomes on some surface, such as the flower scape and bud of ''

Stylidium ''Stylidium'' (also known as triggerplants or trigger plants) is a genus of dicotyledonous plants that belong to the family Stylidiaceae. The genus name ''Stylidium'' is derived from the Greek ''στύλος'' or ''stylos'' (column or pillar), wh ...

'' and ''

'', the

bract In botany, a bract is a modified or specialized leaf, especially one associated with a reproductive structure such as a flower, inflorescence axis or cone scale. Bracts are usually different from foliage leaves. They may be smaller, larger, or o ...

s of ''

Passiflora ''Passiflora'', known also as the passion flowers or passion vines, is a genus of about 550 species of flowering plants, the type genus of the family Passifloraceae. They are mostly tendril-bearing vines, with some being shrubs or trees. The ...

'', and leaves of ''

Roridula ''Roridula'' (; from Latin ''roridus'' "dewy") is a genus of evergreen, insect-trapping shrubs, with two species, of about 1⅓–2 m (4–6⅔ ft). It is the only genus in the family Roridulaceae. It has thin, woody, shyly branching, upright, in ...

''. The trichomes of ''Stylidium'', which appear below the flower, have been known to trap and kill small insects since their discovery several centuries ago, but their purpose remained ambiguous. In November 2006, Dr. Douglas Darnowski published a paper describing the active digestion of proteins when they come in contact with a trichome of a ''Stylidium'' species grown in

aseptic Asepsis is the state of being free from disease-causing micro-organisms (such as pathogenic bacteria, viruses, pathogenic fungi, and parasites). There are two categories of asepsis: medical and surgical. The modern day notion of asepsis is der ...

tissue culture Tissue culture is the growth of tissues or cells in an artificial medium separate from the parent organism. This technique is also called micropropagation. This is typically facilitated via use of a liquid, semi-solid, or solid growth medium, su ...

, proving that the plant, rather than the surface microbes, was the source of protease production. Darnowski asserts in that paper that given this evidence, ''Stylidium'' species are properly called carnivorous, though in order to fulfill the strict definition of carnivory it needs to be proven that they are capable of absorbing nutrients derived from prey and that this adaptation gives the plants some competitive advantage. The glandular hairs on the calyx of plants of the genus

have been proposed as a potential carnivorous adaptation. While these calyxes have long been considered as a seed dispersal mechanism, many researchers have noted the entrapment of numerous ants and other small insects on the species ''

'', '' Plumbago europa'', '' Plumbago indica'', and ''

Plumbago zeylanica ''Plumbago zeylanica'', commonly known as Ceylon leadwort, doctorbush or wild leadwort, is a species of plumbago with a pantropical distribution. Carl Linnaeus described the paleotropical ''P. zeylanica'' and Neotropical ''P. scandens'' as separ ...

''. Studies on ''P. auriculata'' and ''P. indica'' detected potential protease activity from these glands, but were inconsistent in detecting it.

Energy-dispersive X-ray spectroscopy Energy-dispersive X-ray spectroscopy (EDS, EDX, EDXS or XEDS), sometimes called energy dispersive X-ray analysis (EDXA or EDAX) or energy dispersive X-ray microanalysis (EDXMA), is an analytical technique used for the elemental analysis or chemi ...

spectra of the glands on ''P. auriculata'' and ''P. zeylanica'' found that the glandular secretions were composed mainly of the elements C, O, Si, Mg, and Al. One such species, ''P. europaea'', has also been noted to kill small birds by covering them in sticky calyxes, causing them to be unable to fly and subsequently die. A similar sticky-seed killing mechanism has been studied ''

Pisonia grandis ''Pisonia grandis'', the grand devil's-claws, is a species of flowering tree in the ''Bougainvillea'' family, Nyctaginaceae. Description The tree has broad, thin leaves, smooth bark and bears clusters of green sweet-smelling flowers that matu ...

'', but was concluded to not be a carnivorous adaptation. Pameridea

''Roridula'' has a more complex relationship with its prey. The plants in this genus produce sticky leaves with resin-tipped glands that look similar to those of larger '' Drosera''. However, the resin, unlike mucilage, is unable to carry digestive enzymes. Therefore, ''Roridula'' species do not directly benefit from the insects they catch. Instead, they form a mutualistic

symbiosis Symbiosis (from Greek , , "living together", from , , "together", and , bíōsis, "living") is any type of a close and long-term biological interaction between two different biological organisms, be it mutualistic, commensalistic, or para ...

with species of

assassin bug The Reduviidae are a large cosmopolitan family of the order Hemiptera (true bugs). Among the Hemiptera and together with the Nabidae almost all species are terrestrial ambush predators: most other predatory Hemiptera are aquatic. The main example ...

s that eat the trapped insects. The plant benefits from the nutrients in the bugs'

feces Feces ( or faeces), known colloquially and in slang as poo and poop, are the solid or semi-solid remains of food that was not digested in the small intestine, and has been broken down by bacteria in the large intestine. Feces contain a rela ...

. Likewise, the sticky, modified bracts of

passion flowers ''Passiflora'', known also as the passion flowers or passion vines, is a genus of about 550 species of flowering plants, the type genus of the family Passifloraceae. They are mostly tendril-bearing vines, with some being shrubs or trees. They ...

of the section

Dysosmia Dysosmia is a disorder described as any qualitative alteration or distortion of the perception of smell. Qualitative alterations differ from quantitative alterations, which include anosmia and hyposmia. Dysosmia can be classified as either paros ...

have notable glandular bracts that surround flowers and forming fruit. While this has long been discussed as a defense mechanism, studies of ''

Passiflora foetida ''Passiflora foetida'' (common names: stinking passionflower, wild maracuja, bush passion fruit, wild water lemon, stoneflower, love-in-a-mist, or running pop) is a species of passion flower that is native to the southwestern United States (sout ...

'' have investigated them for potential carnivorous abilities. A 1995 paper published in the ''Journal of Biosciences'' detailed the evidence that the glandular bracts played a distinct role in defense of the flower and were also capable of digesting captured prey and absorbing the nutrients. Various authors have questioned the methods and conclusions of this paper. Further studies using on the glandular bracts using

histochemical Histology, also known as microscopic anatomy or microanatomy, is the branch of biology which studies the microscopic anatomy of biological tissues. Histology is the microscopic counterpart to gross anatomy, which looks at larger structures vis ...

tests have confirmed the presence of enzymes in both ''

'' and '' Passiflora sublanceolata''. Various plants of the

Martyniaceae Martyniaceae is a family of flowering plants in the Lamiales order that are restricted to the Americas. The family was included in Pedaliaceae in the Cronquist system (under order Scrophulariales) but is recognized as a separate family by the An ...

family have been considered crude flypaper protocarnivores. Early publications identified the entrapment of numerous insects on the glandular hairs covering the stems and leaves of '' Martynia annua'', '' Proboscidea louisiana'', ''

Proboscidea parviflora ''Proboscidea parviflora'' is a species of flowering plant in the family Martyniaceae known by the common names doubleclaw and red devil's-claw. It is native to the desert southwest of the United States and northern Mexico, where it grows in sand ...

'', and ''

Ibicella lutea ''Ibicella lutea'' (; syn. ''Martynia lutea, Proboscidea lutea'') is a species of flowering plant known by the common name yellow unicorn-plant. It grows in dry conditions, such as those in desert regions. It is native to South America, but has ...

''. Early, rudimentary studies showed that placed bits of food—beef and hard-boiled egg white broke down when placed on the leaf surface of''P. louisiana'' and ''I. lutea'', respectively. Despite this, more recent studies have suggested that there are no detectable

proteases A protease (also called a peptidase, proteinase, or proteolytic enzyme) is an enzyme that catalyzes (increases reaction rate or "speeds up") proteolysis, breaking down proteins into smaller polypeptides or single amino acids, and spurring the for ...

on the leaves of ''I. lutea'' and ''P. louisiana'' and no detectable

phosphatases In biochemistry, a phosphatase is an enzyme that uses water to cleave a phosphoric acid monoester into a phosphate ion and an alcohol. Because a phosphatase enzyme catalyzes the hydrolysis of its substrate, it is a subcategory of hydrolases. P ...

or uptake of N, P, K, Mg from dried flies places on I. lutea and ''P. parviflora''. Observations have suggest that there may be a digestive mutualism between carnivorous insects and the sticky plant surface similar to ''

''. A similar relationship has been identified in many other sticky desert plants and concluded to be a passive defense mechanism.

Pitfall traps

The pitfall traps of protocarnivorous plants are identical to those of carnivorous plants in every way except in the plant's mode of digestion. The rigid definition of carnivory in plants requires digestion of prey by enzymes produced by the plant. Given this criterion, many of the pitfall trap plants commonly considered to be carnivorous would instead be classified as protocarnivorous. However, this is highly contentious and generally not reflected in current carnivorous plant phylogenies or literature. ''

Darlingtonia californica ''Darlingtonia californica'' , also called the California pitcher plant, cobra lily, or cobra plant, is a species of carnivorous plant. It is the sole member of the genus ''Darlingtonia'' in the family Sarraceniaceae. This pitcher plant is nat ...

'' and several '' Heliamphora'' species do not produce their own enzymes, relying instead on an internal food web to break down the prey into absorbable nutrients. Another pitfall trap form unrelated to the Sarraceniaceae family are the urns of

leaves that are formed when leaves are tightly packed together in a rosette, collecting water and trapping insects. Unlike ''

'', which has been proven to produce at least one digestive enzyme and can therefore be considered carnivorous, the epiphytic '' Catopsis berteroniana'' has little evidence supporting the claims that it is carnivorous. It is able to attract and kill prey and the trichomes on the surface of the leaves can absorb nutrients, but so far no enzyme activity has been detected. It may be that this plant also relies on an internal food web for soft tissue digestion. The same could be said for '' Paepalanthus bromelioides'', though it is a member of

Eriocaulaceae The Eriocaulaceae are a family of monocotyledonous flowering plants in the order Poales, commonly known as the pipewort family. The family is large, with about 1207 known species described in seven genera. They are widely distributed, with the ce ...

and not a bromeliad. It also forms a central water reservoir that has adaptations to attract insects. It, like ''C. berteroniana'', produces no digestive enzymes. Another potential protocarnivorous pitfall trap is a species of

teasel ''Dipsacus'' is a genus of flowering plant in the family Caprifoliaceae. The members of this genus are known as teasel, teazel or teazle. The genus includes about 15 species of tall herbaceous biennial plants (rarely short-lived perennial plants ...

, '' Dipsacus fullonum'', which has been only suggested as a possible carnivore. Only one major study has examined ''D. fullonum'' for carnivory and no evidence of digestive enzymes or foliar nutrient absorption was revealed.

Other

Capsella bursa-pastoris ''Capsella bursa-pastoris'', known as shepherd's purse because of its triangular flat fruits, which are purse-like, is a small annual and ruderal flowering plant in the mustard family (Brassicaceae). It is native to eastern Europe and Asia minor, ...

'', Shepherd's purse, is another plant where the claim of carnivory is contested. This unique protocarnivorous plant is only capable of capturing and digesting prey during one stage of its life cycle. The seeds of the plant, when moistened, secrete a

Mucilage Mucilage is a thick, gluey substance produced by nearly all plants and some microorganisms. These microorganisms include protists which use it for their locomotion. The direction of their movement is always opposite to that of the secretion of m ...

that attracts and kills prey. There is also evidence of

activity and absorption of nutrients. More recent studies have suggested that the plants may benefit from the feeding of

Nematodes The nematodes ( or grc-gre, Νηματώδη; la, Nematoda) or roundworms constitute the phylum Nematoda (also called Nemathelminthes), with plant-parasitic nematodes also known as eelworms. They are a diverse animal phylum inhabiting a broa ...

to the seeds of the plants, but due to a small sample size such conclusions cannot be made. Other plants such as ''

Descurainia pinnata ''Descurainia pinnata'' is a species of flowering plant in the family Brassicaceae known by the common name western tansymustard. It is native to North America, where it is widespread and found in varied habitats. It is especially successful in d ...

'', ''

Descurainia sophia ''Descurainia sophia'' is a member of the family Brassicaceae. Common names include flixweed, herb-Sophia and tansy mustard. It reproduces by seeds. It is a dominant weed in dark brown prairie and black prairie soils of southern Alberta. Its s ...

'', ''

Hirschfeldia incana ''Hirschfeldia incana'' (formerly ''Brassica geniculata'') is a species of flowering plant in the mustard family known by many common names, including shortpod mustard, buchanweed, hoary mustard and Mediterranean mustard. It is the only species i ...

'', and '' Lepidium flavum '' were also noted to entrap small insects.

production by seeds is fairly common in the plant kingdom and is typically associated with root and shoot penetration. Further work to identify the nutrient fluxes in this seed-insect system in-situ are required to understand any carnivorous aspects of this system. ''

Puya raimondii ''Puya raimondii'', also known as queen of the Andes (English), titanka (Quechua) or puya de Raimondi (Spanish), is the largest species of bromeliad, its inflorescences reaching up to in height. It is native to the high Andes of Bolivia and Per ...

'' and ''

Puya chilensis ''Puya chilensis'' is a terrestrial bromeliad originating from the arid hillsides of Chile Chile, officially the Republic of Chile, is a country in the western part of South America. It is the southernmost country in the world, and the cl ...

'' are two large arid

bromeliads The Bromeliaceae (the bromeliads) are a family of monocot flowering plants of about 80 genera and 3700 known species, native mainly to the tropical Americas, with several species found in the American subtropics and one in tropical west Africa, ...

that have been suspected of being proto-carnivorous plants due to their entrapment of small animals in their spiney leaves. ''

'' was noted to have associated with numerous birds, some of which would become ensnared in the spikey foliage and die. It is hypothesized that this, as well as dropping from the birds who lived amongst the leaves, are a source of nutrients upon decomposition and subsequent foliage absorption by the plant. Similarly, ''

'' was noted to ensnare livestock such as sheep who, unless rescued would degrade and feed the plant. Despite this, the adaptations seen in ''

Puya Puya may refer to: * ''Puya'' (plant), in the family Bromeliaceae * Puya (river), in Russia * Puya, a variety of Guajillo chili * ''Puya'' (Meitei texts), traditional or mythological texts of the Meetei people * '' Culoepuya'' or ''Culo'e Puya'' ...

'' that lead to ensnarement of animals seems most likely to be a defense mechanism.

Loss of carnivory

A few plants that could be considered protocarnivorous or paracarnivorous are those that once had carnivorous adaptations but appear to be evolving or have evolved away from a direct prey relationship with arthropods and rely on other sources for obtaining nutrients. One example of such a phenomenon is the pitfall trap of ''

Nepenthes ampullaria ''Nepenthes ampullaria'' (; Latin ''ampulla'' meaning "flask") is a very distinctive and widespread species of tropical pitcher plant, present in Borneo, the Maluku Islands, New Guinea, Peninsular Malaysia, Singapore, Sumatra, and Thailand.McPh ...

'', a tropical pitcher plant. Although it retains its ability to attract, capture, kill, and digest insect prey, this species has acquired adaptations that appear to favor digestion of leaf litter. It could potentially be referred to as a

detritivore Detritivores (also known as detrivores, detritophages, detritus feeders, or detritus eaters) are heterotrophs that obtain nutrients by consuming detritus (decomposing plant and animal parts as well as feces). There are many kinds of invertebrate ...

.Clarke, 2001 Another tropical pitcher plant, ''

Nepenthes lowii ''Nepenthes lowii'' , or Low's pitcher-plant,Phillipps, A. & A. Lamb 1996. '' Pitcher-Plants of Borneo''. Natural History Publications (Borneo), Kota Kinabalu. is a tropical pitcher plant endemic to Borneo. It is named after Hugh Low, who discove ...

'', is known to catch very few prey items compared to other ''Nepenthes''. Preliminary observations suggest that this particular species may have moved away from a solely (or even primarily) carnivorous nature and be adapted to "catching" the droppings of birds feeding at its nectaries. A 2009 study found that mature ''N. lowii'' plants derived 57–100% of their foliar nitrogen from

treeshrew The treeshrews (or tree shrews or banxrings) are small mammals native to the tropical forests of South and Southeast Asia. They make up the entire order Scandentia, which split into two families: the Tupaiidae (19 species, "ordinary" treeshre ...

droppings. '' Utricularia purpurea'', a

bladderwort ''Utricularia'', commonly and collectively called the bladderworts, is a genus of carnivorous plants consisting of approximately 233 species (precise counts differ based on classification opinions; a 2001 publication lists 215 species).Salmon, Br ...

, comes from another genus of carnivorous plants and may have lost its appetite for carnivory, at least in part. This species can still trap and digest arthropod prey in its specialized bladder traps, but does so sparingly. Instead, it harbors a community of algae, zooplankton, and debris in the bladders, giving rise to the hypothesis that the bladders of ''U. purpurea'' favor a mutualistic interaction in place of a predator-prey relationship.

Evolution

The disciplines of ecology and evolutionary biology have presented several hypotheses on the evolution of carnivorous plants that may also apply to protocarnivorous plants. The name "protocarnivorous plant" itself suggests that these species are on their way to carnivory, though others may simply be an example of a defense-related adaptation, such as that found in ''

''. Still others (''Utricularia purpurea'', ''Nepenthes ampullaria'', and ''Nepenthes lowii'') may be examples of carnivorous plants moving away from the carnivorous syndrome. In his 1998 book, ''Interrelationship Between Insects and Plants'', Pierre Jolivet only considered four species of plants to be protocarnivorous: ''Catopsis berteroniana'', ''

'', '' B. hectioides'', and ''Paepalanthus bromeloides''. Jolivet writes, "It is important to remember that all carnivorous plants are dicots and all protocarnivorous plants are

monocots Monocotyledons (), commonly referred to as monocots, ( Lilianae '' sensu'' Chase & Reveal) are grass and grass-like flowering plants (angiosperms), the seeds of which typically contain only one embryonic leaf, or cotyledon. They constitute one of ...

," though he does not explain why nor does he describe his reasons for excluding other dicotyledonous plants that are protocarnivorous.Jolivet, 1998

Notes

References

* Adam, J.H. (1997). ''Pertanika Journal of Tropical Agricultural Science'' 20(2/3): 121–134. * * * * * * Clarke, C.M. (1997). ''

Nepenthes of Borneo ''Nepenthes of Borneo'' is a monograph by Charles Clarke on the tropical pitcher plants of Borneo.Clarke, C.M. 1997. ''Nepenthes of Borneo''. Natural History Publications (Borneo), Kota Kinabalu. It was first published in 1997 by Natural History ...

''. Natural History Publications (Borneo), Kota Kinabalu. * Clarke, C.M. (2001). ''

Nepenthes of Sumatra and Peninsular Malaysia ''Nepenthes of Sumatra and Peninsular Malaysia'' is a monograph by Charles Clarke on the tropical pitcher plants of Sumatra, Peninsular Malaysia, and their minor surrounding islands. It was published in 2001 by Natural History Publications (Bor ...

''. Natural History Publications (Borneo), Kota Kinabalu, pp. 59–60. * * * Darwin, Charles. (1875). '' Insectivorous Plants''. J. Murray, London. * * Fahn, A. and Werker, E. (1972). Anatomical mechanisms of seed dispersal. ''in'' Kozlowski, T.T. (ed.), ''Seed Biology'', Academic Press. * * Fountain, H. 2009
A Plant That Thrives When Used as a Toilet
''The New York Times'', June 15, 2009. * Hartmeyer, S. (1998). Carnivory in ''Byblis'' revisited II: The phenomenon of symbiosis on insect trapping plants. ''Carnivorous Plant Newsletter'', 27(4): 110–113. Available online

* * Jaffe, K., Michelangeli, F., Gonzalez, J.M., Miras, B., and Ruiz, M.C. (1992). Carnivory in Pitcher Plants of the Genus ''Heliamphora'' (Sarraceniaceae). ''New Phytologist'', 122(4): 733–744. (First page available online
JSTOR PDF of first page and HTML text of abstract
* Jolivet, Pierre. (1998). ''The Interrelation Between Insects and Plants'', CRC Press. * Juniper, B.E., Robbins, R.J., and Joel, D.M. (1989). '' The Carnivorous Plants''. London: Academic Press. * Lloyd, F.E. (1942). '' The Carnivorous Plants''. New York: The Ronald Press Company. * Mameli, E. (1916). Ricerche anatomiche, fisiologiche e biologiche sulla ''Martynia lutea'' Lindl. ''Atti del'Universita di Pavia'' (Serie 2) 16: 137–188. * Meyers-Rice, B.A. (1999). Testing the appetites of ''Ibicella lutea'' and ''Drosophyllum''. ''Carnivorous Plant Newsletter'', 28: 40–43. Available online
HTML
* * * * Radhamani, T.R., Sudarshana, L., and Krishnan, R. (1995). Defence and carnivory: Dual role of bracts in ''Passiflora foetida''. ''Journal of Biosciences'', 20(5): 657–664. Available online
PDF
* * Schlauer, J. (1997). "New" data relating to the evolution and phylogeny of some carnivorous plant families. ''Carnivorous Plant Newsletter'' 26(2): 34–38 (availabl

. * Schnell, D.E. (2002). ''Carnivorous Plants of the United States and Canada'', second edition. Timber Press. * Simons, Paul. (1981)
How exclusive are carnivorous plants?
''Carnivorous Plants Newsletter'', 10(3):65–68,79-80. * *

Historical observations

Defining carnivory

Degrees of carnivory

Trapping mechanisms

Flypaper traps

Pitfall traps

Other

Loss of carnivory

Evolution

Notes

References

Further reading