evolution of carnivorous and paracarnivorous plants

1. What are carnivorous plants? 4 criteriaHabitatPaper #1 – Phylogeny and structural evolution

• What are paracarnivorous plants?

Digestive mutualismsPaper #2 - RoridulaOther paracarnivores

3. SummaryEvolution of carnivorous and paracarnivorous plants

Outline

“I See You”, man-eating tree of Central/South America.

What are carnivorous plants? “Flesh-eating”; 4 criteria (Lloyd 1976).

2. Trap and killtraps: sticky, pitfall, strategic hairs, waxesdeath: usually drowning, suffocating, some eaten alive

4. Absorb nutrients

3. Digest with endogenous enzymes

Adaptation or coincidence?(i.e. herbivore defense: amber)

more difficult to observe:

• Attract animal prey (old name “insectivorous”)

visual or chemical cuesrange from deceptive mimicry rewards

?

Typical habitat: sunny, moist, nutrient poor

Ombrotrophic – “cloud fed”StagnantAnaerobicAcidic

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

Typical habitat: sunny, moist, nutrient poor

Decreased decompositionDecreased nitrification by bacteria

Increased denitrification by bacteria(nitrogen is lost to the atmosphere)

StagnantAnaerobic

Acidic

Atypical habitat: nutrient poor, semi-arid or epiphytic,

Drosophyllum lusitanicum

Nepenthes veitchii

Pinguicula ramosa

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

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)

4 basic trap types• Flypaper traps F

• Pitcher traps P

• Bladder traps B

• Snap traps S

Structural adaptations: Flypaper traps F

Order Ericales

Order CaryophyllalesOrder Lamiales

(Pinguicula sp.)

Structural adaptations: Pitcher traps P

Order Ericales

Order Poales1 species:

Brocchinia reducta (not in Albert 1992)Order Oxalidales

Order Caryophyllales

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

Structural adaptations: Bladder traps B (1 genus, ~250 spp.)

order Lamialesfamily Lentibulariaceae

Utricularia

Structural adaptations: Snap traps S

Aldrovanda vesiculosa (not in Albert 1992)

Dionaea musipula

order Caryophyllales family Droseraceae

Evolution of carnivorous plants: from Albert 1992 - present

Genlisea

Triphyophyllum

Aldrovanda

Brocchinia

Stevens, P. F., 2008. Angiosperm Phylogeny Website.

1992: 13 genera 4 orders 4 trap types2009: 14 genera 5 orders 5 trap types

Structural adaptations: Lobsterpot traps L (1 genus, 21 spp.)

order Lamialesfamily Lentibulariaceae

Genlisea(not in Albert 1992)

Flypaper traps FPitcher traps PBladder traps BSnap traps SLobsterpot traps L

Structural adaptations: Lobsterpot traps L Genlisea

(not in Albert 1992)

Caryophyllales – family Dioncophyllaceae, Triphyophyllum peltatum (1 sp.)

Evolution of carnivorous plants: from Albert 1992 - present: 5 orders

Ericales: 2 genera, 29 spp.

F

P

Caryophyllales: 6 genera, 298 spp.

F SP Poales: 1 sp.

P

Oxalidales: 1 sp.

P

Lamiales: 4 genera, 252 spp.

F

B

L

Flypaper traps FPitcher traps PBladder traps BSnap traps SLobsterpot traps L Stevens, P. F., 2008. Angiosperm Phylogeny Website.

1992: 13 genera 4 orders 4 trap types2009: 14 genera 5 orders 5 trap types

FS

P

B L

P

P

PF

F


Evolution of carnivorous plants: from Albert 1992 - present: 5 orders

S

B L


Convergent trap types

Evolution: Oxalidales: Cephalotus follicularis (1 sp.)

F

P

P

P

PF

F

S

B L

Ericales: Darlingtonia

Flypaper traps FPitcher traps PSnap traps SBladder traps BLobsterpot traps L


Caryophyllales: 6 genera, 298 spp.

SP

F

F

P

P

P

PF

F

S

B L

Evolution: Caryophyllales - Nepenthes

N. rajafrogs, lizards and ratsup to 3 liters

Evolution: Caryophyllales – Drosophyllum “dewy pine”

Evolution: Caryophyllales – Drosera “sun-dews”

Thigmotropism - oriented growth of an organism in response to mechanical contact


Lamiales: 4 genera, 252 spp.

F

B

L


F

P

P

P

PF

F

S

B L

Evolution: Lamiales – Pinguicula “butterworts”


Ericales: 2 genera, 29 spp.

F

P


F

P

P

P

PF

F

S

B L

Supplemented carnivory: Ericales – Sarracenia and Roridula

supplemented bydigestive mutualismConiine in trap nectar:

same neurotoxin as poison hemlock

endogenous enzymes

Ellison et al. 2003.

Phytotelma inquiline food web

Roridula

Other Ericaleans with

digestive mutualisms:

1. What are carnivorous plants? 4 criteriaHabitatPaper #1 – Phylogeny and structural evolution

• What are paracarnivorous plants?

Digestive mutualismsPaper #2 - RoridulaOther paracarnivores

3. SummaryEvolution of carnivorous and paracarnivorous plants

Outline

“I See You”, man-eating tree of Central/South America.

What are paracarnivorous plants?(aka proto-carnivorous, subcarnivorous, pseudo-carnivorous, part-time carnivorous)

1. Attract 2. Trap/kill 3. Endogenous enzymes

Givnish, 1984

digestive mutualisms

?

What are digestive mutualisms? Darlingtonia californica (1 sp.)

no endogenous enzymes detected

digestive mutualisms:

“digestion by proxy”(exogenous 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).

enzymaticpartners:

bacteriafungi

animals

+ +enzymes rewards

gut bacteria animalsmycorrhizal fungi plants

Paracarnivores with digestive mutualisms: Habitat similarity - sunny, moist, nutrient poor

Paracarnivorous plants treated as carnivorous in Albert 1992

Proboscidea

Heliamphora

Darlingtonia

digestive mutualism

digestive mutualism

Paracarnivores with digestive mutualisms: Habitat similarity

Guiana highlands, Venezuela

Paracarnivorous plants with digestive mutualisms: Heliamphora

D’Amato, Peter, 1998. The Savage Garden

(no endogenous enzymes found)


frog digestive mutualism suspected, no experimental data

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.


Paracarnivore or true carnivore? Brocchinia reducta

Isley, Paul,1987. Tillandsia.

digestive mutualism(pseudoscorpions)

4. Absorb?

but endogenous enzymes?

Givnish, 1984.

Digestive enzymes

Plachno et al. 2006. Fluorescence labeling of phosphatase activity in digestive glands of carnivorous plants. Plant Biology.

weak endogenous enzymes

Endogenous enzymes found in carnivorous plants?

•amylase (starch)•chitinase (also fungal and arthropod defense, barley seeds...)•esterase•lipase •peroxidase•phosphatase (also respiration, dephosphorylation...)•protease (i.e. nepenthacine “similar to pepsin”)•ribonuclease

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?)

Paracarnivory - Paper #2: Roridula: 2 sp. R.gorgonias, R. dentata

digestive mutualism

larger prey microhabitat

gut bacteria animalsmycorrhizal fungi plants

+ +enzymes rewards

?

Paracarnivore or true carnivore? Roridula

glue

Anderson et al., 2007. Density-dependent outcomes in a digestive mutualism between carnivorous Roridula plants and their associated hemipterans


Anderson et al., 2002. It takes two to tango but three is a

tangle: mutualists and cheaters on the carnivorous plant Roridula.

but endogenous enzymes?


Plachno et al. 2006.

Roridula


Anderson B, 2005. Adaptations to foliar absorption of faeces: a pathway in plant carnivory.

(+ absorption via cuticular gaps)


Paracarnivore or true carnivore? Lamiales: Byblis

+ suspected digestive mutualism (also hemipteran feces), currently not studied?


Other fecally supplemented carnivores – Nepenthes lowii

Clarke, Charles, 1997.Nepenthes of Borneo.

At least 2 digestive mutualists(no experimental data)

3.sunbirds4.inquiline crane fly larvae

mimicry?

(tendril domatium)

Other fecally supplemented carnivores – Nepenthes bicalcarata

digestive mutualisms?

Paracarnivores or true carnivores? Catopsis and Paepalanthus

Catopsis berteroniana

Paepalanthus bromelioides(no endogenous enzymes detected)

(no endogenous enzymes detected)

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 "carnivorous"?

(no enzyme data)

Darnowski, et. al., 2006. Evidence of protocarnivory in triggerplants (Stylidium spp.; Stylidiaceae).

Paracarnivores or true carnivores? Stylidium

absorption not detected

questionably detected protease...

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.

Puya raimondii and Pisonia grandis: avian-specific paracarnivores?!

L?

Rees et al., 1978. Puya raimondii (Pitcairnioideae, Bromeliaceae) and birds: an hypothesis on nutrient relationships.

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 thesea for 12 d or more (as might be experienced by seedsattached 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?

Summary

Carnivorous Non-carnivorous• Convergent evolution

• Alternative nutrient pathways, cost/benefits of carnivory

• Phytotelmata inquiline food web dynamics (discrete boundaries, easily manipulated)

• Coevolution, stability, assemblage of digestive mutualisms, the role of fungal and

bacterial digestive mutualists

The end

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.

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?

evolution of carnivorous and paracarnivorous plants

Documents

paracarnivorous plants

criteria habitat paper

typical habitat

digestive mutualisms

animal preyold

acostbenefit modelfor

chemical cues

strategic hairs