Protocarnivorous plant

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A protocarnivorous plant (sometimes also paracarnivorous, subcarnivorous, or borderline carnivore), according to some definitions and unlike a true carnivorous plant, lacks the ability to either digest or absorb nutrients from insects or animals that are trapped and killed by the plant's morphological adaptations such as sticky trichomes or pitfall traps. The traps of protocarnivorous plants parallel the trap structures of confirmed carnivorous plants.

Some authors prefer the term "protocarnivorous" because it implies that these plants are on the evolutionary path to true carnivory, while others oppose the term for the very 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.^[1]

The demarcation between carnivorous and protocarnivorous is blurred by the lack of a strict definition of botanical carnivory and ambiguous 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.

Contents 1 Defining carnivory 2 Degrees of carnivory 3 Trapping mechanisms 3.1 Flypaper traps 3.2 Pitfall traps 3.3 Other 4 Evolution 5 Notes 6 References

[edit] Defining carnivory

Defining what criteria a plant must meet in order to be considered a carnivorous plant has yielded two distinct proposed definitions: one with strict requirements and the other less restrictive.

The strict set of requirements dictate that a plant must possess morphological adaptations that attract prey through scent or visual cues, capture and retain prey (i.e. the waxy scales of Brocchinia reducta or downward facing hairs of Heliamphora prevent escape), digest the dead prey through enzymes produced by the plant, and adsorb the products of digestion through specialized structures. The presence of commensals is also listed as strong evidence of a long evolutionary history of carnivory.^[2] By this definition, many sun pitcher plants (Heliamphora),^[3] a North American pitcher plant (Sarracenia purpurea),^[4] and the cobra lily (Darlingtonia californica)^[5] would not be included on a roster of carnivorous plants because they rely on symbiotic bacteria and other organisms to produce the necessary proteolytic enzymes.

The broader definition is less strict and does not require plants to produce their own enzymes for digestive purposes. This definition also incorporates requirements for adaptations or resource allocations that result in the active attraction, capture, and/or digestion of prey. It, too, requires adsorption of the now digested nutrients, but also notes that the plant must receive some noticeable benefit from the carnivorous syndrome. That is, the plant must display some significant increase in fitness because of the nutrients obtained from its carnivorous adaptations (i.e. increased growth rate, increased chance of survival, higher pollen production or seed set).^[6]

[edit] 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 (a rose, for example) to fully carnivorous plants with active trapping mechanisms like those of Dionaea or Aldrovanda. 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 and phosphorous seen where true carnivorous plants grow.^[7] The function of the protocarnivorous habit, however, need not be directly related to lack of nutrient access. Some classic protocarnivorous plants represent convergent evolution in form but not necessarily in function. Plumbago, for example, possesses glandular trichomes on its calyces that structurally resemble the tentacles of Drosera and Drosophyllum.^[8] The function of the Plumbago tentacles is, however, disputed. Some contend that their intended purpose is to aid in pollination, adhering seeds to visiting pollinators.^[9] Others note that on some species (Plumbago auriculata), small crawling insects have been trapped in the Plumbago's mucilage, leading to 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.^[8]

[edit] Trapping mechanisms

There are visible parallels between the trapping mechanisms of carnivorous plants and protocarnivorous plants. Plumbago 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 the fact that they do not produce their own digestive enzymes. There are also protocarnivorous bromeliads that form a pitfall trap in an "urn" of rosetted leaves that are held together tightly. Then there are 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.

[edit] Flypaper traps

Dr. George Spomer of the University of Idaho has discovered protocarnivorous activity and function in several glandular plant species, including Cerastium arvense, Gilia aggregata, Heuchera cylindrica, Mimulus lewisii, Penstemon attenuata, Penstemon diphyllus, Potentilla glandulosa var. intermedia, Ribes cerum, Rosa nutkana var. hispida, Rosa woodsia var. ultramontana, Solanum tuberosum, Stellaria americana, and Stellaria jamesiana. These species tested positive for protease activity, though it is unclear whether the protease is produced by the plant or by surface microbes. Two additional species evaluated by Dr. Spomer, Geranium viscossisimum and Potentilla arguta, exhibited protease activity and were further examined with ¹⁴C-labeled algal protein for nutrient absorption activity. Both of these latter species displayed a capability to digest and absorb the ¹⁴C-labeled algal protein.^[10]

Other plants that have sticky trichomes on some surface, such as the flower scape and bud of Stylidium and Plumbago,^[11] the bracts of Passiflora foetida, and leaves of Roridula, are considered to be protocarnivorous. 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, however, 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 tissue culture, proving that the plant was the source of protease production and not created by a surface microbe.^[12] 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.

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 with species of assassin bug that eat the trapped insects. The plant benefits from the nutrients in the bugs' feces.^[13]

Likewise, the sticky, modified bracts of Passiflora foetida have been investigated for their carnivorous ability. 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.^[14]

Ibicella lutea is another flypaper protocarnivore that has been the subject of several studies. Early studies concluded that the plant digested proteinaceous offerings, though the methods were crude.^[15] Subsequent studies done more carefully tested for the presence of protease activity and found none, though it was noted that the plant has a great capacity for capturing and killing prey.^[16]

[edit] 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 criteria, many of the pitfall trap plants commonly considered to be carnivorous would instead be classified as protocarnivorous. Sarracenia purpurea,^[4] Darlingtonia californica,^[5] and several Heliamphora species do not produce their own enzymes, relying on an internal food web to break down the prey into absorbable nutrients.^[3]

Another pitfall trap form unrelated to the Sarraceniaceae family are the urns of bromeliad leaves that are formed when leaves are tightly packed together in a rosette, collecting water and trapping insects. Unlike Brocchinia reducta, 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 and it may be that this plant also relies on an internal food web for soft tissue digestion.^[17] The same could be said for ‎Paepalanthus bromelioides, though it is a member of Eriocaulaceae 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.^[18]

Another potential protocarnivorous pitfall trap is a species of teasel, Dipsacus fullonum, and has only been 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.^[19]

[edit] Other

Another pitfall trap in its own right is that of Nepenthes ampullaria, a tropical pitcher plant. While 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.^[20] A different tropical pitcher plant, Nepenthes lowii, is known to catch very few prey items compared to other Nepenthes.^[21] 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.^[22][20]

Utricularia purpurea, a bladderwort, comes from another genus of confirmed carnivorous plants and has lost its appetite for carnivory. This species can still trap and digest insect prey in its specialized bladder traps, but rarely does so. Instead, it harbors a community of algae, zooplankton, and debris in the bladders, giving rise to the hypothesis that the bladders of U. purpurea have a mutualistic interaction in place of a predator-prey relationship.^[23]

Capsella bursa-pastoris, shepherd's purse, is another plant where the claim of carnivory is contested. This unique protocarnivorous plant is only capable of capturing prey during one stage of its life cycle. The seeds of the plant, when moistened, secrete a viscous fluid that actively attracts and kills prey. Evidence has also been presented to support the claim that there is protease activity and absorption of nutrients.^[24] The only carnivory criteria not explored is how much the plant benefits from the carnivorous adaptation.^[1]

[edit] Evolution

Main article: Carnivorous plant#Ecology and modelling of carnivory

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 Plumbago.^[8][9] 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, Brocchinia reducta, B. hectioides, and Paepalanthus bromeloides. Jolivet writes, "It is important to remember that all carnivorous plants are dicots and all protocarnivorous plants are monocots," though he does not explain why.^[25]

[edit] Notes

[edit] References