Protocarnivorous plant

A protocarnivorous plant (sometimes also paracarnivorous, subcarnivorous, or borderline carnivore), according to some definitions, traps and kills insects or other animals but lacks the ability to either directly digest or absorb nutrients from its prey like a carnivorous plant. The morphological adaptations such as sticky trichomes or pitfall 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, 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.^[1]

The demarcation between carnivorous and protocarnivorous is blurred by the lack of a strict definition of

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

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

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),^[9] 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.^[9]

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

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 phosphorus seen where true carnivorous plants grow.^[10] 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.^[11] The function of the Plumbago tentacles is, however, disputed. Some contend that their function is to aid in pollination, adhering seeds to visiting pollinators.^[12] Others note that on some species (Plumbago auriculata), 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.^[11]

Trapping mechanisms

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

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

The glandular hairs on the calyx of plants of the genus Plumbago have been proposed as a potential carnivorous adaptation. While these calyxes have long been considered as a seed dispersal mechanism,^[16] many researchers have noted the entrapment of numerous ants and other small insects on the species Plumbago auriculata,^[17] Plumbago europa,^[18] Plumbago indica,^[19] and Plumbago zeylanica.^{[20][citation needed]} Studies on P. auriculata and P. indica detected potential protease activity from these glands,^[19] but were inconsistent in detecting it. Energy-dispersive X-ray spectroscopy 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.^[21] 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.^[22] A similar sticky-seed killing mechanism has been studied Pisonia grandis, but was concluded to not be a carnivorous adaptation.^[23]

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

Likewise, the sticky, modified bracts of

histochemical tests have confirmed the presence of enzymes in both Passiflora foetida and Passiflora sublanceolata.^[28]

Various plants of the

phosphatases or uptake of N, P, K, Mg from dried flies places on I. lutea and P. parviflora.^[34] Observations have suggested that there may be a digestive mutualism between carnivorous insects and the sticky plant surface similar to Roridula.^[35] A similar relationship has been identified in many other sticky desert plants and concluded to be a passive defense mechanism.^[36]

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.^[37][38] Darlingtonia californica^[8] 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.^[7]

Another pitfall trap form unrelated to the

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. It may be that this plant also relies on an internal food web for soft tissue digestion.^[39] 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.^[40]

Another potential protocarnivorous pitfall trap is a species of teasel, 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.^[41]

Other

Hirschfeldia incana, and Lepidium flavum were also noted to entrap small insects.^[44] Mucilage

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.

bromeliads that have been suspected of being proto-carnivorous plants due to their entrapment of small animals in their spiney leaves. Puya raimondii 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.^[45] Similarly, Puya chilensis was noted to ensnare livestock such as sheep who, unless rescued would degrade and feed the plant.^[46] Despite this, the adaptations seen in Puya that lead to ensnarement of animals seems most likely to be a defense mechanism.^[47]

Loss of carnivory

leaf litter

.

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

leaf litter. It could potentially be referred to as a detritivore.^[48] Another tropical pitcher plant, Nepenthes lowii, is known to catch very few prey items compared to other Nepenthes.^[49] 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.^[48][50] A 2009 study found that mature N. lowii plants derived 57–100% of their foliar nitrogen from treeshrew droppings.^[51][52]

Utricularia purpurea, a bladderwort, 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.^[53]

Evolution

Further information: 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.^[11][12] 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,

monocots," though he does not explain why nor does he describe his reasons for excluding other dicotyledonous plants that are protocarnivorous.^[54]

Notes

1. ^ ^{a b} Schnell, 2002
2. ^ Darwin, 1875
3. PMID 29973685
   .
4. ^ Lloyd, 1942
5. ^ Simons, 1981
6. ^ The five rigid criteria of the carnivorous syndrome proposed by Juniper et al. (1989) and Albert et al. (1992).
7. ^ ^{a b} 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).
8. ^ ^{a b} 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 of bacteria, protozoa, mites, and fly larvae" to break down captured prey (Naeem, 1988; Nielsen, 1990).
9. ^
   S2CID 84947503{{citation}}: CS1 maint: multiple names: authors list (link
   )
10. ^ Spoomer (1999) presented the argument that carnivorous plants may have evolved from protocarnivorous species when faced with a nutrient deficiency, noting the genetic evidence for multiple independent plant lines that evolved a fully carnivorous habit (Juniper et al., 1989; Albert et al., 1992).
11. ^ ^{a b c} Schlauer, 1997
12. ^ ^{a b} Fahn and Werker, 1972
13. ^ Spomer, 1999
14. ^ Rachmilevitz and Joel, 1976
15. ^ Darnowski et al., 2006
16. ISBN 9780124243019
    .
17. ^
    S2CID 222324082
    .
18. ^ Heim, F (1898). The Biological Relations Between Plants and Ants.
19. ^ ^{a b} Stoltzfus, A.; Suda, J.; Kettering, R.; Wolfe, A.; Williams, S. (2002). "Secretion of digestive enzymes in Plumbago". In Proceedings: The 4th International Carnivorous Plant Conference (203–207).
20. PMID 25957315
    .
21. ^ Chaudhari, S. S.; Chaudhari, G. S. (2017). "Comparative LM and SEM studies of glandular trichomes on the calyx of flowers of two species of Plumbago Linn". Plant Archives. 17 (2): 948–954.
22. ^ Purger, J. J.; Kletecki, E.; Trócsányi, B.; Muzinic, J.; Purger, D.; Széles, G. L.; Lanszki, J (2012). "The Common Leadwort Plumbago europaea L. as a natural trap for the wintering Goldcrests Regulus regulus: a case study from Adriatic islands". Journal of Biological Research. 17 (176).
23. S2CID 86457740
    .
24. ^ Hartmeyer (1998) described this phenomenon in the genus Roridula.
25. doi:10.1111/curt.12050
    .
26. ^ Passiflora foetida bracts produce proteases and acid phosphatases (Radhamani et al., 1995).
27. doi:10.1111/j.1095-8339.2009.01014.x
    .
28. ^ de Lemos, R. C. C. (2017). "Anatomia, ultraestrutura e química das glândulas foliares de Passiflora L. (Passifloraceae)". Doutorado em Botânica, Universidade de São Paulo.
29. ^ Crawford, J. (1884). "Martynia and its Hublme Servants". American Journal of Pharmacy (1835–1907): 641.
30. doi:10.5962/bhl.part.29234
    .
31. ^ ^{a b} Mameli, E (1916). "Ricerche anatomiche, fisiologiche e biologiche sulla Martynia lutea Lindl". Atti dell'Universita di Pavia. 2 (16).
32. ^ Fermi, C; Buscaglioni, D (1899). "The proteolytic enzymes in the plant kingdom". ZBL. Bakt., II. Abbot (5): 24–27.
33. S2CID 248093742
    .
34. PMID 19556266
    .
35. S2CID 247121501
    .
36. PMID 23205839.{{cite journal}}: CS1 maint: multiple names: authors list (link
    )
37. PMID 25538295
    .
38. PMID 25948113.{{cite journal}}: CS1 maint: multiple names: authors list (link
    )
39. ^ Frank and O'Meara (1984) detected a higher trapping rate in C. berteroniana compared to three other tank bromeliads. They also noted that commensals lived unharmed within the tank. Benzing et al. (1976) discovered that C. berteroniana is capable of absorbing radioisotope-tagged amino acids through the leaves.
40. ^ Pierre Jolivet (1998) suggests that this plant also relies on its internal food web to break down the soft tissues of prey for absorption.
41. ^ Christy (1923) did note that the fluid collected in the basin formed by the leaves has a lower surface tension, which could be an adaptation to kill prey.
42. ^ Barber, 1978
43. PMID 29973685.{{cite journal}}: CS1 maint: multiple names: authors list (link
    )
44. ^ Reeves, E. L., & Garcia, C. (1969). "Mucilaginous seeds of the Cruciferae family as potential biological control agents for mosquito larvae". Mosq. News (29): 601–607.{{cite journal}}: CS1 maint: multiple names: authors list (link)
45. doi:10.1139/b80-157.{{cite journal}}: CS1 maint: multiple names: authors list (link
    )
46. ^ "Sheep-Eating Plant Opens Up After 15 Years : DNews". DNews. Archived from the original on 2015-11-21. Retrieved 2015-11-30.
47. doi:10.1111/j.1095-8339.2009.01014.x.{{cite journal}}: CS1 maint: multiple names: authors list (link
    )
48. ^ ^{a b} Clarke, 2001
49. ^ Adam, 1997
50. ^ Clarke, 1997
51. ^ Clarke et al., 2009
52. ^ Fountain, 2009
53. ^ Richards (2001) did an extensive study in the field on U. purpurea and noted that trapping rates of the usual Utricularia prey were significantly lower than in other species in the genus.
54. ^ Jolivet, 1998

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Further reading

• Rice, B.A. (2011). "What exactly is a carnivorous plant?". Carnivorous Plant Newsletter. 40 (1): 19–23.
  S2CID 247016538
  .