Evolution of Carnivorous and Paracarnivorous Plants

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Plant-Animal Interactions graduate seminar Spring 2009 with Dr. Ed Connor

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  • The first part of my talk will be an overview of what technically defines a carnivorous plant . I was surprised there is actually disagreement over this but it makes sense when you see that’s it’s not black and white . Then I want to go into the evolution of carnivorous plants. I chose this paper because it’s the most recent molecular phylogenetic study to try and synthesize the research, but it was done in 1992 and only has a few of the 600+ species... For the second part I want to describe some of the plants that are considered not-quite carnivorous, because I think it is through these plants that we can better understand how the carnivorous trait evolved in general, and as you’ll see, it’s actually quite fuzzy and ill-defined. “ I See You” man-eating tree of Central/South America.
  • So first, what defines something as carnivorous? It has to be “flesh-eating” But To be technically carnivorous, a plant has to be able to attract animal prey, kill it, and digest and absorb nutrients from the animal’s flesh . The majority of prey are insects, but carnivorous plants have also been known to eat spiders, protists, rotifers, frogs, lizards, rats . These distinctions are important because as we’ll see with the paracarnivores there are many variations of these 3 criteria.
  • Quickly: where do they grow? Sunny moist sites (except Drosophyllum Dewy Pine alkaline Mediterranean) Nutrient poor, mostly nitrogen . Sources of nitrogen in nature. Nitrogen is critical for building amino acids, and therefore needed for protein and DNA. Uncommon in epiphytes due to moisture restrictions (photosynthesis cost/benefit in Brocchinia paper), whereas ant mutualisms common. Barthlott 2007: “ 6 of themost important nutrients to plants are contained in insects in the following compositions: 10.5% nitrogen 3.2% potassium 2.3% calcium 0.6% phosphorous 0.09% magnesium 0.02% iron” Sarracenia only absorbs nitrogen and phosphorous Christensen 1976 Schulze 1991 found that N uptake varies as much as 25% in Cephalotus to 75% in Darlingtonia Bog preservation 400 B.C. Tollund man due to high tannins and anaerobic
  • Decomposition in bogs is extremely slow, hence there are few available nutrients that are cycling through this system. Nitrogen cycle conversion of nitrogen to nitrates by bacteria; (2) the extraction of the nitrates by plants and the building of amino acids and proteins by adding an amino group to the carbon compounds produced in photosynthesis; (3) the ingestion of plants by animals, and (4) the return of nitrogen to the soil in animal excretions or on the death and decomposition of plants and animals. Denitrification During anaerobic (low oxygen) conditions, denitrification by bacteria occurs. This results in nitrates being converted to nitrogen gases (NO, N 2 O, N 2 ) and returned to the atmosphere . Nitrate can also be reduced to nitrite and subsequently combine with ammonium in the anammox process, which also results in the production of dinitrogen gas.
  • But there are also Drosophyllum lusitanicum (only one species, order Caryophyllales, family Drosophyllaceae) With Roridula??
  • Ericoid? cite
  • 1992 Bignoniales is now Lamiales This shows 4 of the 5 trap types and only __ of the __genera, including only 4 of the 5 carnivorous orders
  • Flypaper examples – leaf epidermal outgrowths , many plants have evolved glandular trichomes usually as an herbivore defense . As Albert points out, two types of stalks
  • Pitcher examples – epidasciation? Fusion of leaves. many plants may incidentally collect water, called phytotelm , which may accumulate both plant and animal debris. Phytotelm is interesting because there is often a whole community of organisms that have evolved to live in this microhabitat, bacteria, fungi, tree frogs that spend their whole life in it, even crabs... Nepenthes raja – frogs, lizards and rats, 3 Liters , (Cheek Jebb 2001, Clark).
  • Other traps: Utricularia (unknown origin) “ And may we regard the Australian types of Utricularia as ancient types and in some measure as analogs of ancient animal forms of that continent?” (Lloyd 1942)
  • Another example of leaf fusion traps: Snap traps – Aldrovanda (not in Albert) (find flower) and Dionaea Flower only stays open for a few hours Said to be the most widely distributed carnivorous plant, but rare in it’s region...
  • Genlisia (chemical traps, modified stem or leaf? Habitat?) Lobster traps are
  • So this is basically the same phylogeny presented in the paper but at the order level and it includes all angiosperms and gymnosperms (?), taken from the APG website. Nearly all species are split between in Cary and Lam. This implies carnivory may have evolved as few as 5 times...
  • So this is basically the same phylogeny presented in the paper but at the order level and it includes all angiosperms and gymnosperms (?), taken from the APG website. Nearly all species are split between in Cary and Lam. This implies carnivory may have evolved as few as 5 times...
  • convergence
  • So this is basically the same phylogeny presented in the paper but at the order level and it includes all angiosperms and gymnosperms (?), taken from the APG website. Nearly all species are split between in Cary and Lam. This implies carnivory may have evolved as few as 5 times...
  • Thigmatropic –basically as you saw in the animation at the beginning, these plants are capable of surround prey with digestive fluids and basically create a temporary stomach . How? Turgidity? Have two different types of glands secreting two things/
  • So this is basically the same phylogeny presented in the paper but at the order level and it includes all angiosperms and gymnosperms (?), taken from the APG website. Nearly all species are split between in Cary and Lam. This implies carnivory may have evolved as few as 5 times...
  • So this is basically the same phylogeny presented in the paper but at the order level and it includes all angiosperms and gymnosperms (?), taken from the APG website. Nearly all species are split between in Cary and Lam. This implies carnivory may have evolved as few as 5 times...
  • Ellison et al. 2003.
  • The first part of my talk will be an overview of what technically defines a carnivorous plant . I was surprised there is actually disagreement over this but it makes sense when you see that’s it’s not black and white . Then I want to go into the evolution of carnivorous plants. I chose this paper because it’s the most recent molecular phylogenetic study to try and synthesize the research, but it was done in 1992 and only has a few of the 600+ species... For the second part I want to describe some of the plants that are considered not-quite carnivorous, because I think it is through these plants that we can better understand how the carnivorous trait evolved in general, and as you’ll see, it’s actually quite fuzzy and ill-defined. “ I See You” man-eating tree of Central/South America.
  • Some say “protocarnivorous” or “subcarnivorous”, but those terms imply a more ancestral form of a true carnivore. Only some grow on nutrient poor habitat… One or more criteria missing (usually replaced by digestive mutualisms ) digestive mutualism with bacteria, fungi, aquatic arthropods, crustaceans, birds FAECES
  • pseudoscorpions
  • About all the enzyme types Mucilage: polar glycoprotein Resin: hydrocarbon (often terpenes)
  • Digestive mutualism -
  • 1. Supplemented carnivory: Nepenthes ampullaria appears to have moved away from the direct food-prey relationship with arthropods; it has pitfall traps that can catch and digest insects, but it has also added the ability to digest leaf litter. 2. Utricularia purpurea (bladderwort) also can trap and digest insects, but most (?) if it’s nutrients come from the community of algae, zooplankton, and debris that it harbors in its water bladder, which may indicate a mutualistic interaction. 3. Sarracenia purpurea, for example, there are few enzymes and nutrients from the entrapped animales are made available to the plant by the activity of detritivores that break up the prey that is further decomposed by bacteria, in turn eaten by rotifers and protozoa and ultimately by mosquito larvae - all forming a microcosm in the liquid of each pitcher (Kitching 2000; Ellison et al. 2003; Butler & Ellison 2007). Caterpillars of the moth Exyra fax drain the pitchers by opening up a hole at the base; they then consume the pitcher.
  • berteroniana
  • But did not sterilize!
  • Puya raimondii and Pisonia: avian-specific traps?
  • Evolution of Carnivorous and Paracarnivorous Plants

    1. 2. <ul><li>What are carnivorous plants? </li></ul><ul><ul><li>4 criteria </li></ul></ul><ul><ul><li>Habitat </li></ul></ul><ul><ul><li>Paper #1 – Phylogeny and structural evolution </li></ul></ul><ul><li>What are paracarnivorous plants? </li></ul><ul><ul><li>Digestive mutualisms </li></ul></ul><ul><ul><li>Paper #2 - Roridula </li></ul></ul><ul><ul><li>Other paracarnivores </li></ul></ul><ul><li>Summary </li></ul><ul><ul><li>Evolution of carnivorous and paracarnivorous plants </li></ul></ul>Outline “ I See You”, man-eating tree of Central/South America.
    2. 3. What are carnivorous plants? “Flesh-eating”; 4 criteria (Lloyd 1976). 2. Trap and kill traps : sticky, pitfall, strategic hairs, waxes death : usually drowning, suffocating, some eaten alive 4. Absorb nutrients 3. Digest with endogenous enzymes more difficult to observe: Adaptation or coincidence? (i.e. herbivore defense: amber) <ul><li>Attract animal prey (old name “insectivorous”) </li></ul><ul><ul><li>visual or chemical cues </li></ul></ul><ul><ul><li>range from deceptive mimicry  rewards </li></ul></ul>?
    3. 4. Typical habitat : sunny, moist, nutrient poor Ombrotrophic – “cloud fed” Stagnant Anaerobic Acidic Givnish, 1984. Carnivory in the bromeliad Brocchinia reducta , with a cost/benefit model for the general restriction of carnivorous plants to sunny, moist, nutrient-poor habitats. Rare: <0.2% of all plants
    4. 5. Typical habitat : sunny, moist, nutrient poor Decreased decomposition Decreased nitrification by bacteria Increased denitrification by bacteria (nitrogen is lost to the atmosphere) Stagnant Anaerobic Acidic
    5. 6. Atypical habitat: nutrient poor, semi-arid or epiphytic , Drosophyllum lusitanicum Nepenthes veitchii Pinguicula ramosa
    6. 7. Early carnivorous plants? Archaeamphora longicervia Li, Hongqi, 2005. Early Cretaceous sarraceniacean-like pitcher plants from China. Hess, 2005. Evidence of Zoophagy in a Second Liverwort Species, Pleurozia purpurea
    7. 8. Structural evolution: Paper #1 - Albert et al. 1992 rbcL - ~1000 bp Rubisco - highly conserved 13 carnivorous genera in 4 orders (Note: Bignoniales has been collapsed into Lamiales) <ul><li>4 basic trap types </li></ul><ul><li>Flypaper traps F </li></ul><ul><li>Pitcher traps P </li></ul><ul><li>Bladder traps B </li></ul><ul><li>Snap traps S </li></ul>
    8. 9. Structural adaptations: Flypaper traps F Order Ericales Order Caryophyllales Order Lamiales ( Pinguicula sp.)
    9. 10. Structural adaptations: Pitcher traps P Epiascidiation : inrolling and fusion of leaves (pseudo-stomach?) Phytotelma : fluid collected in a plant structure (rainwater, digestive enzymes) aka pitfall traps – floral mimicry , nectar lure, slippery surface wax, downward pointing hairs Order Ericales Order Poales 1 species: Brocchinia reducta (not in Albert 1992) Order Oxalidales Order Caryophyllales
    10. 11. Structural adaptations: Bladder traps B (1 genus, ~250 spp.) order Lamiales family Lentibulariaceae Utricularia
    11. 12. Structural adaptations: Snap traps S order Caryophyllales family Droseraceae Aldrovanda vesiculosa (not in Albert 1992) Dionaea musipula
    12. 13. Evolution of carnivorous plants: from Albert 1992 - present Stevens, P. F., 2008. Angiosperm Phylogeny Website . 1992: 13 genera 4 orders 4 trap types 2009: 14 genera 5 orders 5 trap types Genlisea Triphyophyllum Aldrovanda Brocchinia
    13. 14. Structural adaptations: Lobsterpot traps L (1 genus, 21 spp.) order Lamiales family Lentibulariaceae Genlisea (not in Albert 1992) Flypaper traps F Pitcher traps P Bladder traps B Snap traps S Lobsterpot traps L
    14. 15. Structural adaptations: Lobsterpot traps L Genlisea
    15. 16. (not in Albert 1992) Caryophyllales – family Dioncophyllaceae, Triphyophyllum peltatum (1 sp.)
    16. 17. Evolution of carnivorous plants: from Albert 1992 - present : 5 orders Flypaper traps F Pitcher traps P Bladder traps B Snap traps S Lobsterpot traps L Stevens, P. F., 2008. Angiosperm Phylogeny Website . 1992: 13 genera 4 orders 4 trap types 2009: 14 genera 5 orders 5 trap types Ericales : 2 genera, 29 spp. F P Caryophyllales: 6 genera, 298 spp. F S P Poales : 1 sp. P Oxalidales : 1 sp. P Lamiales: 4 genera, 252 spp. F B L
    17. 18. F S P B L P P P F F Flypaper traps F Pitcher traps P Bladder traps B Snap traps S Lobsterpot traps L Evolution of carnivorous plants: from Albert 1992 - present : 5 orders S B L Flypaper traps F Pitcher traps P Bladder traps B Snap traps S Lobsterpot traps L Convergent trap types
    18. 19. Evolution: Oxalidales: Cephalotus follicularis (1 sp.) F P P P P F F S B L Ericales: Darlingtonia
    19. 20. Flypaper traps F Pitcher traps P Snap traps S Bladder traps B Lobsterpot traps L Evolution of carnivorous plants: from Albert 1992 - pr esent Caryophyllales: 6 genera, 298 spp. S P F F P P P P F F S B L
    20. 21. Evolution: Caryophyllales - Nepenthes N. raja frogs, lizards and rats up to 3 liters
    21. 22. Evolution: Caryophyllales – Drosophyllum “dewy pine”
    22. 23. Evolution: Caryophyllales – Drosera “sun-dews” Thigmotropism - oriented growth of an organism in response to mechanical contact
    23. 24. Evolution of carnivorous plants: from Albert 1992 - present Lamiales: 4 genera, 252 spp. F Flypaper traps F Pitcher traps P Bladder traps B Snap traps S Lobsterpot traps L F P P P P F F S B L B L
    24. 25. Evolution: Lamiales – Pinguicula “butterworts”
    25. 26. Evolution of carnivorous plants: from Albert 1992 - present Flypaper traps F Pitcher traps P Bladder traps B Snap traps S Lobsterpot traps L F P P P P F F S B L Ericales : 2 genera, 29 spp. F P
    26. 27. Supplemented carnivory: Ericales – Sarracenia and Roridula supplemented by digestive mutualism Coniine in trap nectar: same neurotoxin as poison hemlock endogenous enzymes Ellison et al. 2003. Phytotelma inquiline food web Roridula Other Ericaleans with digestive mutualisms :
    27. 28. <ul><li>What are carnivorous plants? </li></ul><ul><ul><li>4 criteria </li></ul></ul><ul><ul><li>Habitat </li></ul></ul><ul><ul><li>Paper #1 – Phylogeny and structural evolution </li></ul></ul><ul><li>What are paracarnivorous plants? </li></ul><ul><ul><li>Digestive mutualisms </li></ul></ul><ul><ul><li>Paper #2 - Roridula </li></ul></ul><ul><ul><li>Other paracarnivores </li></ul></ul><ul><li>Summary </li></ul><ul><ul><li>Evolution of carnivorous and paracarnivorous plants </li></ul></ul>Outline “ I See You”, man-eating tree of Central/South America.
    28. 29. What are paracarnivorous plants? (aka proto-carnivorous, subcarnivorous, pseudo-carnivorous, part-time carnivorous) Givnish, 1984 digestive mutualisms ? 1. Attract 2. Trap/kill 3. Endogenous enzymes
    29. 30. What are digestive mutualisms? Darlingtonia californica (1 sp.) no endogenous enzymes detected digestive mutualisms: “ digestion by proxy” ( ex ogenous enzymes) (Bacteria) Slime mites: Sarraceniopus darlingtoniae Midge larvae: Metriocnemus edwardsi (Fungi) Spiders Fashing, 2004. Biology of Sarraceniopus darlingtoniae (Histiostomatidae: Astigmata), an obligatory inhabitant of the fluid-filled pitchers of Darlingtonia californica (Sarraceniaceae).
    30. 31. + + enzymes   rewards gut bacteria   animals mycorrhizal fungi   plants Paracarnivores with digestive mutualisms : Habitat similarity - sunny, moist, nutrient poor enzymatic partners : bacteria fungi animals
    31. 32. Paracarnivorous plants treated as carnivorous in Albert 1992 digestive mutualism digestive mutualism Proboscidea Heliamphora Darlingtonia
    32. 33. Paracarnivores with digestive mutualisms : Habitat similarity Guiana highlands, Venezuela
    33. 34. Paracarnivorous plants with digestive mutualisms : Heliamphora D’Amato, Peter, 1998. The Savage Garden (no endogenous enzymes found) Guiana highlands, Venezuela frog digestive mutualism suspected, no experimental data
    34. 35. Paracarnivore or true carnivore? Brocchinia reducta Givnish, 1984 . Carnivory in the bromeliad Brocchinia reducta , with a cost/benefit model for the general restriction of carnivorous plants to sunny, moist, nutrient-poor habitats. Guiana highlands, Venezuela
    35. 36. Paracarnivore or true carnivore? Brocchinia reducta digestive mutualism (pseudoscorpions) 4. Absorb? but endogenous enzymes? Givnish, 1984. Isley, Paul,1987. Tillandsia .
    36. 37. Digestive enzymes Plachno et al. 2006 . Fluorescence labeling of phosphatase activity in digestive glands of carnivorous plants . Plant Biology . weak endogenous enzymes <ul><li>Endogenous enzymes found in carnivorous plants? </li></ul><ul><li>amylase (starch) </li></ul><ul><li>chitinase (also fungal and arthropod defense, barley seeds...) </li></ul><ul><li>esterase </li></ul><ul><li>lipase </li></ul><ul><li>peroxidase </li></ul><ul><li>phosphatase (also respiration, dephosphorylation...) </li></ul><ul><li>protease (i.e. nepenthacine “similar to pepsin”) </li></ul><ul><li>ribonuclease </li></ul>
    37. 38. Paracarnivory - Paper #2: Roridula: 2 sp. R.gorgonias, R. dentata Dolling WR, Palmer JM. 1991 . Pameridea (Hemiptera: Miridae): predaceous bugs specific to a highly viscid plant genus Roridula . Pameridea: 2 sp. P. roridulae, P. marlothi (+ pollination mutualism?)
    38. 39. digestive mutualism Paracarnivore or true carnivore? Roridula larger prey microhabitat gut bacteria   animals mycorrhizal fungi   plants + + enzymes   rewards ? glue
    39. 40. Anderson et al., 2007 . Density-dependent outcomes in a digestive mutualism between carnivorous Roridula plants and their associated hemipterans Paracarnivore or true carnivore? Roridula but endogenous enzymes? Anderson et al., 2002 . It takes two to tango but three is a tangle: mutualists and cheaters on the carnivorous plant Roridula .
    40. 41. Paracarnivore or true carnivore? Roridula Plachno et al. 2006 .
    41. 42. Roridula Plachno et al. 2006 . Paracarnivore or true carnivore? Roridula Anderson B, 2005. Adaptations to foliar absorption of faeces : a pathway in plant carnivory. (+ absorption via cuticular gaps)
    42. 43. Paracarnivore or true carnivore? Lamiales : Byblis + suspected digestive mutualism (also hemipteran feces ), currently not studied? Plachno et al. 2006 .
    43. 44. Other fecally supplemented carnivores – Nepenthes lowii Clarke, Charles, 1997. Nepenthes of Borneo. <ul><li>At least 2 digestive mutualists </li></ul><ul><li>(no experimental data) </li></ul><ul><li>sunbirds </li></ul><ul><li>inquiline crane fly larvae </li></ul>mimicry?
    44. 45. (tendril domatium) Other fecally supplemented carnivores – Nepenthes bicalcarata digestive mutualisms?
    45. 46. Paracarnivores or true carnivores? Catopsis and Paepalanthus Catopsis berteroniana Paepalanthus bromelioides (no endogenous enzymes detected) (no endogenous enzymes detected)
    46. 47. Radhamani, et. al., 1995. Defence and carnivory: Dual role of bracts in Passiflora foetida . Paracarnivores or true carnivores? Passiflora and Capsella questionably detected protease... Barber, J.T., 1978. Capsella bursa-pastoris seeds: Are they &quot;carnivorous&quot;? (no enzyme data)
    47. 48. Darnowski, et. al., 2006. Evidence of protocarnivory in triggerplants ( Stylidium spp.; Stylidiaceae) . Paracarnivores or true carnivores? Stylidium absorption not detected questionably detected protease...
    48. 49. Floral traps? Or herbivore defense? Plumbago (no enzyme or absorption data) Spomer, G.G.,1999. Evidence of protocarnivorous capabilities in Geranium viscosissimum and Potentilla arguta and other sticky plants.
    49. 50. Puya raimondii and Pisonia grandis : avian-specific paracarnivores?! L ? Rees et al., 1978 . Puya raimondii (Pitcairnioideae, Bromeliaceae) and birds: an hypothesis on nutrient relationships .
    50. 51. Puya raimondii and Pisonia grandis : avian-specific paracarnivores?! “ The fate of carcasses and seeds attached to carcasses” 22 bird carcasses were monitored daily . Scavengers usually found the carcasses within a day, and 91% were dismembered. The mean time to dismemberment was 3.3 days “ ...no seeds tolerated prolonged immersion in the sea for 12 d or more (as might be experienced by seeds attached to a dead bird floating on the sea )” “ Although birds killed by entanglement add nutrients to the soil, the amounts would be trivial compared with the massive inputs from guano, failed eggs and dead chicks. ” “ Seeds attached to carcasses did not have improved germination or survival.” Burger, A, 2005 . Dispersal and germination of seeds of Pisonia grandis , an Indo-Pacific tropical tree associated with insular seabird colonies F ?
    51. 52. Summary <ul><li>Convergent evolution </li></ul><ul><li>Alternative nutrient pathways , cost/benefits of carnivory </li></ul><ul><li>Phytotelmata inquiline food web dynamics (discrete boundaries, easily manipulated) </li></ul><ul><li>Coevolution , stability , assemblage of digestive mutualisms , the role of fungal and bacterial digestive mutualists </li></ul>Carnivorous Non-carnivorous
    52. 53. The end
    53. 54. Over 600 species of plants in 13 families have evolved adaptations to enable them to attract, trap, kill, digest and absorb animal prey. Although Darwin referred to these plants as “insectivorous”, they have been known to catch small frogs, fish, and even rats. These plants may use visual or chemical attractants to lure their victims, and occasionally even offer nectar as bait. What are carnivorous plants? Where do they grow? Carnivorous plants grow in nutrient poor habitats that are usually sunny and water logged. A common misconception is that they only grow in the tropics - many species are native to North America, and Utricularia can be found in Siberian bogs. Carnivorous plants are found where plant growth is limited by a lack of nutrients, especially nitrogen, which is necessary for DNA synthesis and abundant in plant and animal tissue.
    54. 57. Brocchinia reducta Native to highly leeched soils in the Guiana highlands, the leaves of Brocchinia are rolled into a tube shape that collects rainwater, and crawling insects slip on the waxy surface, fall in, and drown. This method of “pitfall” trap is found in true carnivorous plants, which fill this fluid with digestive enzymes. Rather than enzymes, Brocchinia is thought to rely on predators such as pseudoscorpions, as well as microorganisms, to digest their prey.m Roridula gorgonias Scientists have long speculated whether or not Roridula should be considered a true carnivore. This is because although Roridula readily traps insects on its sticky hairs, plants in the wild rely on a mutualism with an insect, Pameridia, which patrols the plant and feeds on the trapped prey. Roridula appears to derive most of its nitrogen not from the prey directly, but from the nitrogen-rich feces of Pameridia , and so is often considered a “paracarnivorous” plant. Carnivorous or Paracarnivorous?

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