- Welcome everyone to Wednesday Nite @ the Lab,
I'm Tom Zinnen, I work here
at the UW-Madison Biotechnology Center.
I also work for UW-Extension Cooperative Extension.
And on behalf of those folks and are other co-organizers,
Wisconsin Public Television, Wisconsin Alumni Association,
and the UW-Madison Science Alliance.
Thanks again for coming to Wednesday Nite @ the Lab.
We do this every Wednesday night 50 times a year.
Tonight is my pleasure to introduce to you, Tom Givnish.
And he's from the Department of Botany.
He was born in Philadelphia,
and then he went to La Salle College High School,
which is a stacked noun, which I love.
So that was the high school for La Salle College.
Absolutely. Then he went to Princeton.
How far is Princeton from Philadelphia?
- 50 miles. - (whistles) Close.
And at Princeton University, he studied math undergrad
and stayed on there at Princeton to get his PhD in Biology.
And then he went to teach at Harvard,
and in 1985, he came to UW-Madison.
Tonight he's going to talk about one of the cool things ever.
Plants that eat animals: Carnivorous plants.
Is that fair enough?
He's going to talk about, "The Green Empire Strikes Back:
"The Ecology and Evolution of Carnivorous Plants."
Please join me welcoming Tom Givnish back
to Wednesday Nite @ the Lab. (audience applauding)
- Thanks so much. - I appreciate it.
- Thanks for those very kind words,
Tom, I hope you'll find it a very fun topic
we'll be discussing tonight.
As you most plant species are eaten,
in whole or part, by animals that act as leaf eaters,
or pollinators or seed dispersers,
but carnivorous plants have turned the tables,
and consume animals as prey.
Charles Darwin was the first to recognize,
and ultimately strongly defend,
this remarkable fact, beginning in 1860.
He was walking through an open, acid,
heath on wet, sandy peat in Southern England,
when he was surprised to see the great number of insects
caught by the glistening leaves of the common sundew,
which is a low-growing herb.
The sticky droplets secreted by the red glandular hairs,
or tentacles on each leaf, glitter in the sun like dew,
which gives sundews their name,
and sundews entrap insects that range
from small flies to larger butterflies and damselflies.
Given the large number of sundews present in any given site,
Darwin saw that, quote, "The number of insects
"thus annually slaughtered must be prodigious."
(audience laughing) Close quote.
Now Darwin realized that the sticky hairs of many plants,
like petunias, kill insects
without the plants receiving any benefit
other than protection against being eaten by those insects.
But he was able to show,
through a series of careful
observations and brilliant experiments,
culminating in his classic 1875 book
on "Insectivorous Plants,"
that sundews and a few other carnivores differ
in having extraordinary adaptations
to entrap and digest insects.
His son, Francis, soon thereafter demonstrated that sundews
that caught prey grew faster and set more seeds
than those that had not.
Given how little nitrate is available to roots in acid,
wet peat, Darwin argued that carnivorous plants
should gain an advantage on those soils
by augmenting their nitrogen supply via insect capture.
Darwin demonstrated three crucial facts about sundews.
First, their tentacles
are exquisitely sensitive to pressure,
and minute doses of nitrogenous liquids.
Secondly, the tentacles, and in some species,
the leaves themselves, you can see here,
move quickly, over seconds to minutes,
toward entrapped insects, further ensnaring them.
Finally, the tentacles secrete fluids
that digest nitrogenous substances,
and then later resorb them.
Today, we can visualize these extraordinary movements,
and secretions and resorptions
through time-lapse photography,
enzyme assays, and...
Microcopy to trace the movement
of labeled proteins or amino acids
into plant tissues and cell compartments.
But Darwin didn't have the luxury
of access to such sophisticated approaches,
and instead had to rely on his own drawings and a stopwatch,
the fate of minute pieces of cooked egg white
and meat exposed to secretions,
and the microscopic examination of tentacle cells
as they resorbed the digest.
Now through this, Darwin is able to document
or infer the mechanism of prey capture
in seven genera of carnivorous plants.
These included the sundews of the genus Drosera,
with 200 species worldwide.
I was just actually in the great center of diversity
for this genus in Southwest Australia
that has about 2/3 of all the species in the world.
These sundews bear active sticky traps with tentacles,
and often leaves that move over seconds to minutes.
And then also the closely related single species
of Venus flytrap, Dionaea,
restricted to a small area
in the coastal plain of the Carolinas.
These bear snap-trap leaves
with two lobes bearing nectaries,
and as you can see here, trigger hairs nearby.
These lobes will close in less than a second
when an insect touches at least two of the trigger hairs
in quick succession.
The widely spaced teeth or cilia
allow small insects to escape while, as you can see,
retaining larger prey as the lobes clamp shut.
The closed leaf lobes form a tight chamber
in which the prey is digested.
And the leaf re-opens after digestion is completed,
resetting the trap.
Recent studies have shown that the Venus flytrap
actually counts the electrical spikes
caused by touching individual trigger hairs,
with rapid trap closure driven
by voltage-regulated ion channels,
for sodium and potassium
and calcium, that begin transmitting electrical signals
within tens of milliseconds after stimulation.
These cause the leaf lobes to clamp shut,
and increasingly so, as the prey struggles
within the trap touching the trigger hairs
and it does through a welter of processes
that we still don't fully understood
but almost surely involve water movement,
and rapid cell wall growth, believe it or not,
and a bi-stable lobe geometry
will flip from concave to convex very rapidly.
Electromechanical stimuli also release jasmonate,
which is a hormone involved in responses to insect attack
used by most other plants, but in Venus flytrap,
it triggers the release of digestive enzymes
over tens of minutes to days.
While Darwin did not understand
the precise mechanism by which Drosera and Dionaea
rapidly close their traps, he was able to show
that some kind of impulse traveled through their tissues.
Understandably, he became quite enthused
with all these discoveries, he considered the Venus flytrap
to be the, quote unquote,
"the most wonderful plant in the world"
and he even wrote to a colleague at the time
that quote: "At the present moment,
"I am more interested in Drosera
"than the origin of all the species in the world!"
(audience applauds)
Coming in 1860, just after the origin of species
that's saying a lot.
By the way, by comparison Li-nay-ass,
responding to some very early reports of possible carnivory
that he received in the 18th century said it's impossible
that if plants were to eat animals,
it would contravene the will of God,
(audience laughs) and he dismissed it out of hand.
Now the waterwheel plant, Aldrovanda,
has a patchy distribution worldwide
and essentially is a miniature aquatic version of Dionaea,
with snap traps that close very rapidly underwater,
and capture insect larvae, crustaceans, and even small fish.
Butterworts in the genus Pinguicula,
including about 100 species in the northern hemisphere,
have yellow, glandular leaves and inrolled leaf margins
that serve as active sticky traps to catch small flies.
The single species of dewy pine, Drosophyllum,
from the western Mediterranean, has glandular leaves,
but these glands and leaves
do not move and so they form passive sticky traps.
By the way, dewy pines are relatives of sundews,
they are not pines.
Pines are coniferous, not carnivorous.
(audience applauds) All right.
Corkscrew plants.
Many of you I'm sure have never heard of these,
of the genus Genlisea,
30 species of butterwort relatives from tropical Africa
and the Americas, bear strange forked roots.
Actually they are leaves, in water or wet sand,
and each of them bears, as you can see,
spiral grooves with the hairs all aligned
up toward where the roots join and there's a mouth
that then leads to
a passage way through a series of cones
arranged more or less like a lobster pot or an eel trap
and apparently ensnares protozoa, and cyanobacteria,
nematodes, micro-crustaceans, especially copepods,
mites, and unicellular algae.
The prey are sort of like Shmoos.
I don't know how many people remember
the old Al Capp cartoons involving L'il Abner,
but the Shmoos threw themselves into the frying pan
and these guys swing themselves into the stomach of the plant.
Finally, bladderworts in the genus Utricularia,
with 250 species worldwide,
have unique, underwater suction traps.
We now know that these bladder-like organs
have four-sided, or four-armed, pardon me, glands,
so that plant really has four arms
that are inside that pump water out
and create a partial vacuum inside,
and then a trap door,
shown here, which is perched on a raised threshold.
Now if a small aquatic animal jostles the door
or the antennae coming off the door,
it slips past the threshold,
the pressure outside forces the water in,
zips in and stage two, brings the prey in with it
and then immediately snaps shut right after that.
Now, as shown by this clip which shows a crustacean
initially swimming behind the ladder,
this all happens in a very short period of time,
indeed only a few milli-- (scoffs) There it was!
(audience applauds) In just a few milliseconds.
Almost looks like a quantum effect, one time it's inside,
one time it's outside, and it's a very rapid movement,
much faster than the Venus flytrap,
and it required the invention of high-speed cameras to study.
Digestions begins soon after the bladders snap shut.
Now Darwin's closest friend and colleague, Joseph Hooker, he's the guy on the right.
He was the director of Kew Gardens,
first described carnivory
in pitcher plants in the genus Nepenthes
in an address published to support Darwin's ideas.
Nepenthes has about 150 species
in Old World tropical forests,
and its pitcher-like leaves serve as pitfall traps
in which insects are attracted to nectaries
around the pitcher's rim or what's called peristome.
We'll be revisiting this a number of times later tonight.
They slip on that rim or a waxy zone just below it,
they drown, and then are digested in the pitcher fluid.
Darwin only briefly mentioned this plant in his book,
as well as New World pitcher plants,
Sarracenia and Darlingtonia,
that had been studied in very brief form
by the American botanist Mark Canby.
These 10 genera, Drosera and Dionaea,
Aldrovanda, Pinguicula, Droso-phyllum, Genlisea,
Utricularia, Nepenthes, Sarracenia and Darlingtonia,
form the carnivorous plant canon, and for many decades,
these were the only plants considered to be carnivorous.
Remarkably, Darwin, and his successors,
never offered a formal definition of such plants,
and that impeded the discovery and study of new carnivores.
In 1984, I proposed a definition based on two criteria.
First, carnivorous plants must be able
to absorb nutrients from dead animals,
and thereby benefit in growth, survival, or reproduction.
Second, they must have one or more unequivocal adaptations
for prey capture, attraction, or digestion.
Adaptations for all three of these processes are not required,
as evidenced by pitcher plants that lack digestive glands,
and bladderworts that lack attractants.
The requirement for adaptations for prey attraction,
capture, or digestion, is needed to separate carnivores
from just every other every-day plant,
given that earthworms and nematodes,
and all manner of microbes
are constantly dying in the soil,
and their nutrients absorbed by the roots of plants.
It turns out my definition has been widely adopted,
and, based on it, we now recognize over 800 species
of carnivorous plants in five orders,
19 genera and 12 families.
Now carnivorous plants may seem to be oddities,
but they raise many fundamental questions.
How frequently have they evolved independently,
when and under what circumstances?
What are the physiological and ecological tradeoffs
that restrict such plants to some nutrient-poor environments
but not others, like epiphytic perches.
And how do the advantages of carnivory differ
from those of other unusual mechanisms
of capturing nutrients?
What fraction of their nutrient budget
do carnivorous plants obtain from prey,
and how does that affect their ability to photosynthesize?
How do traps develop?
What shifts in trap structure have evolved within lineages,
and how are they related to species ecology?
What special kinds of adaptations do plants have to capture,
and benefit from animal prey?
And what kinds of genomic changes
have become associated with the--
are associated with the evolution of botanical carnivory?
I going to address many of these questions today,
giving the greatest attention to the costs and benefits
of the carnivorous habit and what that implies
about where carnivorous plants should be dominant,
and some of the really remarkable strategies
that carnivorous plants have recently been shown to pursue.
Now, over the last several years,
several new groups of carnivorous plants
have been documented by myself,
and several other scientists, including two,
species of two bromeliad genera,
and one pipewort, each with pitfall traps;
Roridula, from south Africa,
which depends on pamerid bugs to eat
and digest insects that have been trapped by the plants,
and then excrete nutrient-rich wastes onto the plant.
And the remarkable Philcoxia from Brazil,
with tiny leaves just below white sand that trap nematodes.
We've also learned that several carnivorous plants
have evolved further to capture nutrients
by acting as bivouacs
or latrines for non-prey animals,
or to recruit insects, to act as butlers
to maintain the traps and keep them functioning.
In some cases, we know now that carnivorous plants
have co-opted genes that are normally used
to defend against herbivores, like jasmonates,
or to absorb of nutrients in the roots
and these genes are instead expressed in the trap leaves.
They are used to transduce signals to move trap components
and secrete enzymes, and then resorb digests.
So thanks to modern molecular phylogenetics,
by which we can deduce evolutionary relationships
among species rigorously from divergences
in their DNA sequences, we now know that carnivorous plants
have evolved at least 10 times, independently,
over the past two to 85 million years.
Just a few months ago, my colleagues,
and I used sequence data
across all orders of flowering plants
to place all the lineages currently know
of carnivorous plants in the angiosperm family tree,
and we calibrated that tree against time
using the ages of two dozen fossils.
The three most recent origins of carnivory,
over the past 1.9 to 2.7 million years,
occurred in the monocot order Poales,
and involve a few species
in otherwise non-carnivorous genera of bromeliads and pipeworts;
all of them involve pitfall traps formed by multiple leaves,
rather than the highly-specialized pitfall traps formed
by individual leaves in the more ancient lineages
of pitcher plants among the rest of the flowering plants.
I discovered one of these new groups
of carnivorous plants many years ago,
in the bromeliad genus Brocchinia.
Two species...
they're on the right of course,
have cylindrical rosettes of bright yellow leaves
that impound rainwater.
Their inner surfaces are coated with a fine waxy dust
that readily exfoliates so that insects lose their footing,
and fall into the tank.
The tank fluid is highly acidic, has a nectar-like scent,
and contains, as you can see,
numerous bodies of dead ants or bees.
The leaf bases are studded with umbrella-like,
absorptive hairs or trichomes,
that absorb amino acids and mineral nutrients at high rates.
The two carnivorous species of Brocchinia
dominate several ecosystems atop the rainy
and extremely infertile tepuis,
or sandstone table mountains of southern Venezuela.
These are The Lost Worlds of Conan Doyle,
which I, and my colleagues visited on foot,
and by helicopter.
We showed that Brocchinia has a greater diversity
of specialized mechanisms of nutrient capture
than any other genus of flowering plants,
including carnivory, nitrogen fixation, the ant-fed habit,
potentially a frog-fed tree and tank epiphytes
that capture fallen plant material.
We used DNA variation to infer the phylogeny
or family tree of Brocchinia and trace its adaptive radiation
in nutrient-capture strategies.
The evolution of tightly overlapping bases
that impound rainwater in tanks,
and of absorptive leaf trichomes, were the key innovations
that led to the evolution of carnivory, shown here in red,
the ant-fed habit shown in blue,
the frog-fed habit shown in green,
and epiphytism shown as you can see in blue.
Now six of the remaining seven origins of carnivorous plants
occurred in, what we call,
the asterids and caryophyllids among the dicots
or if you know recent developments
in plant systematic, the eudicots.
And many of these asterids and caryophyllids
bear glandular hairs, apparently defensive in nature.
Darwin argued that such hairs were the first step
toward the evolution of carnivory.
The largest and oldest of these groups,
within the order Nepenthales,
includes about 400 carnivorous species,
about 1/2 the total, arose 86 million years ago,
including plants with a remarkable range of trap mechanisms,
including active sticky traps in Drosera,
passive sticky traps in Drosophyllum and Triphyophyllum,
snap traps in Dionaea and Aldrovanda,
and pitfall traps in Nepenthes.
All of them in one order.
Of course they had 86 million years to do this.
This phylogeny suggests that carnivory in the lineage
arose associated with passive sticky traps
akin to the defensive hairs
seen in the non-carnivorous Nepenthales,
that are sister to the carnivores,
and that led to the rise ultimately of active sticky traps
in the sundews, snap traps, the Venus flytrap,
and the waterwheel plant and pitfall traps in Nepenthes,
loss of carnivory in the adult stage of Triphyophyllum
in tropical rainforests and then complete loss of carnivory
in several related vines in tropical rainforests.
Many species of Nepenthes,
and tropical vines occur in rainy climates
that would rinse away secretions from glandular hairs,
rendering sticky traps inviable, and it was also,
by the way, provide abundant fluid which to fill
the pitchers of Nepenthes.
The sticky traps of Drosera and Drosophyllum
generally are found in climates that are substantially drier
and hence less likely to wash the secretions away.
The second largest lineage of carnivorous plants,
including over 300 species in family Lentibulariaceae
the butterwort family, in the order Lamiales,
the mints and their relatives,
evolved 43 million years ago,
and includes highly divergent mechanisms for prey capture.
These include active sticky traps
in the butterworts at the top,
the eel traps in corkscrew plants in the middle,
and then the suction traps in the bladderworts.
Homology, let's say the evolutionary similarities
among these trap types remain elusive.
The hope is that by identifying the genes expressed
in developing operational trap leaves,
we will resolve this long-standing puzzle
in the near future.
Pitcher plants evolved in three separate lineages:
Nepenthes in the order Nepenthales
in the Asian, Madagascar and Pacific tropics;
Sarracenia, Darlingtonia and Heliamphora in the Americas;
and Cephalotus in Southwestern Australia.
Their pitchers are remarkably convergent in several features,
especially in the prominently grooved lip, or peristome,
that arose independently in Cephalotus and Nepenthes.
This convergence has occurred despite different parts
of the pitchers having been derived,
being homologous, in other words,
different organs in different lineages.
In Nepenthes and Sarraceniaceae,
the pitcher lid appears to be derived from a leaf apex,
a leaf tip, while in Cephalotus, the pitcher body,
is derived from the leaf tip,
while the lid is derived from the leaf body,
so the Cephalotus pitcher is upside-down
in terms of its homology relative to the other two families.
Let's turn next to the ecology of carnivorous plants,
where some of the most remarkable findings
in the past several years have occurred.
In his pioneering book on insectivorous plants,
Darwin devoted only a few lines
to their potential ecological advantage,
stating that the absorption of animal matter
from captured insects explains how Drosera can flourish
in extremely poor peaty soils,
considering the nature of the soil where it grows,
the supply of nitrogen would be extremely limited,
or quite deficient, unless the plant had the power
of obtaining this important element from captured insects.
Darwin thus explained why carnivorous plants
occur on nutrient-poor sites
but otherwise said very little about the functional
or ecological significance of carnivory.
It was not until 1984 that my colleagues and I outlined
the first cost/benefit model that addressed
the context-specific value of carnivory in detail.
Over the intervening years,
this model has provided a conceptual framework
for dozens of studies
on the ecophysiology of carnivorous plants,
of their ecological distribution,
and of the pathways to their evolution.
Today, I will briefly review, and re-assess this model,
discuss how it can be extended,
as we have done just in the last few months,
and evaluate the degree
to which its assumptions and predictions
have been supported.
The traps of carnivorous plants
provide an alternative source of nutrients,
but also involve the costs,
the energetic cost of lures and digestive enzymes,
of nutrient resorption, of tract activation and resetting,
and of photosynthetically inefficient leaves.
To determine when carnivorous plants should evolve
or be favored competitively, we must compare these costs
with the energetic benefits of carnivory.
Carnivory should be favored whenever the energetic benefits
of a small investment in carnivory exceed the costs.
Our 1984 model assumed that advantages
in energy capture translate into advantages in competition,
and thus, to advantages in fitness,
the rate of production of viable offspring.
We also assumed that the initial trap structure
was a simple phenotypic step from ancestral forms.
No matter what the energetic
or fitness advantage of carnivory,
it's very unlikely that mutations encoding a complex trap
could arise all at once.
Given these assumptions, selection within species
or competition among species should favor carnivory
whenever the initial marginal benefit obtained via carnivory
measured as increased rates of photosynthesis
per unit leaf mass, exceed its marginal cost
of constructing traps, measuring the same units of carbon.
Carnivory might provide, as you can see on this table,
four kinds of energetic benefits,
involving, first, an increased rate of photosynthesis
per unit leaf mass; second, an increased rate of conversion
of photosynthate to new leaf tissue;
third, reduction of allocation
to unproductive roots; and fourth, partial replacement
of autotrophy and photosynthesis with heterotrophy;
that is say, energy capture by eating other organisms.
Now uptake of nitrogen, phosphorus, or other nutrients
via carnivory could result in benefits one, two, or three,
leading to increased concentrations of RuBisCO
or other photosynthetic enzymes in new leaf tissue,
increased stores of nutrients to convert stocks
of carbohydrates into new leaves,
or decreased demand for nutrients provided by the roots.
Many studies show that feeding
does enhance the growth of carnivorous plants,
especially under nutrient-poor conditions,
but few have tested the proposed elevation
of photosynthesis by feeding.
The strongest support for feeding
leading to higher levels of foliar nitrogen and phosphorus,
and therefore higher photosynthetic rates in new leaves,
supporting hypothesis one,
was provided by Farnsworth and Ellison
for 10 Sarracenia species,
and by Pavlovic et al. for Drosera capensis.
And you can see in both cases
that feeding benefits growth
and also in this case, you can see that the benefit
is greater in sunnier environments as you'd expect
given that RuBisCO is more limiting to growth
and to photosynthesis in sun than in shade.
Now, we know now based on a variety of studies
that Carnivorous plants get 6% to 100%
of their leaf nitrogen, and phosphorus supplies, from prey.
Experimental tests of hypothesis two
have not yet been conducted.
Some support for hypothesis three
comes from comparative data indicating
that carnivores often have
smaller roots
than non-carnivores.
And finally, most of the evidence
argues against hypothesis four:
terrestrial plants mostly obtain nutrients
and not carbon from carnivory,
although some carbon uptake occurs in a few cases,
probably because of the absorption of amino acids.
The situation might be different though
for aquatic bladderworts,
which often allocate very little biomass to leaves,
and can grow in complete darkness
if they're supplied with a carbohydrate-rich medium.
Let's consider plants of a given size,
and ask whether a small allocation to carnivory
would increase their net growth, and, thus, competitive ability.
As the amount of energy invested in carnivory rises,
to the right, costs should rise proportionally
in its C-curve.
In addition, prey capture, nutrient absorption,
and thus the rate of photosynthesis,
or conversion of photosynthate to new leaves,
should increase, as shown by that top curve, B,
rising, rapidly at first, but then plateauing,
with increasing investments in carnivory
as the efficiency of prey capture
or the conversion of nutrients
to enhance photosynthesis or more leaf mass declines.
For the moment, we're going to assume that root allocation
doesn't vary with allocation to carnivory.
And under those assumptions, carnivory should be favored
whenever the initial slope of the benefits curve
exceeds that of the cost curve;
that is, when the benefits of small initial investment
in carnivory exceed the costs.
The dash lines indicate the difference
between the cost and the benefits
and the optimal investment in carnivory
should occur right at the point that maximizes
the difference between the benefit and cost curves,
where their slopes, in other words, are equal.
Photosynthesis is unlikely to rise
with allocation to carnivory unless nutrients
are in short supply, so the greatest net benefit
of carnivory should occur on nutrient-poor sites.
Indeed, the usual increase in the growth
of carnivorous plants when supplied with prey,
seen in 17 of 20 studies reviewed recently,
disappeared in almost all cases
when the substrate was fertilized.
If light or moisture are in limited supply,
then they should also reduce the extent
by which nutrient capture via carnivory
can elevate carbon gain. Let me just go back here.
So that's the lower curve in shady or dry circumstances,
less of a benefit.
In addition, we'd expect that rich soils
should elevate photosynthesis
but eliminate almost all further gains
that could be due to carnivory.
Consequently, we reached the conclusion
that carnivory is most likely to be favored
on sites that are sunny and moist as well as nutrient-poor,
in agreement with the habitats
actually occupied by almost all carnivorous plants.
And this goes beyond what Darwin had explained in the past.
What kinds of habitats are nutrient-poor?
Wet soils are mostly deficient in available nitrogen,
either nitrate or ammonium,
due to anoxia reducing nitrogen fixation,
root function and decomposition.
Bogs are precipitation-fed and wet,
and thus deficient in both phosphorus,
it usually comes out of the weathering of a rock,
as well as nitrogen.
Our Wisconsin bogs harbor one species of pitcher plant,
several species each of the sundews
and of the bladderworts.
Ancient, highly leached sands are also deficient
in phosphorus and nitrogen,
accounting for highly infertile soils
in boreal and maritime areas
that have high rainfall relative to evaporation,
supporting a lot of carnivorous plants.
As well as, lots of carnivorous plants
in the Atlantic and Gulf Coastal Plains of the US,
on very wet sandy soils,
the tepuis of the Guayana Shield that I mentioned earlier,
and ancient sandstone landscapes of South Africa shown here,
Southwestern Australia,
where my students and I were just a couple weeks ago,
and in Borneo, all of them are hot spots
for carnivorous plant diversity.
Paradoxically, highly calcareous soils...
Oh, let's just see it, have I? I guess I've skipped over something here.
There we go.
Highly calcareous soils over limestone or dolomite
are cation-rich, but often support a lot
of butterworts, and we think this may be
because they're actually phosphorus deficient,
the calcium carbonate complexes with phosphorus,
and that may account for the abundance
of butterworts on limestone.
Based on tissue stoichiometry,
the ratios of N, P, and K,
most terrestrial carnivorous plants appear to be limited
by N or P or N and P.
By contrast, Aldrovanda and some bladderworts
appear to be limited by potassium, by K, which may reflect,
the large potassium requirements for constructing
and pumping water from their aquatic traps.
A second prediction of our economic model is that
fire over wet, infertile substrates should favor carnivory.
Frequent fires can further impoverish soil fertility
by volatilizing the leaf nitrogen in the tissue burned,
and they increase light levels and soil moisture
by removing competing foliage,
doing all that, they favor carnivory.
Many carnivorous plants are indeed associated strongly
with nutrient-poor, moist habitats that burn frequently.
Examples include, as shown here,
Drosera, Sarracenia, Pinguicula, and Dionaea
on fire-swept pocosins, and low-lying pine savannas
of the Southern Atlantic Coastal Plain;
Darlingtonia in serpentine fens kept open by fire
in the Siskiyou Mountains in Oregon and California;
Brocchinia, Heliamphora and Drosera
on fire-swept, wet sandy savannas
on tepuis in Southern Venezuela; Roridula, and Drosera
on fire-swept damp fynbos in South Africa;
and Byblis, Drosera, and Cephalotus in fire-swept kwongan,
and reed-swamps in Southwestern Australia.
Seed germination in Byblis,
the plant at the bottom,
is even driven by smoke!
Germination is enhanced by chemicals in smoke.
Other forms of disturbance over sterile substrates,
including logging, lake drainage,
or fractures or landslides that expose bare rock,
can also favor carnivores without, of course,
volatilizing N.
A third prediction of our economic model
is that Epiphytism works against carnivory
and favors myrmecotrophy.
That's being fed by ants.
Perches on tree boles and branches are nutrient-poor
and often sunny, but are also episodically dry,
and thus unlikely to support carnivorous plants.
Only 17 epiphytic species are carnivores,
far fewer than that expected
given the number of carnivorous species
and epiphytic species overall.
Almost all of these epiphytic carnivores
are Utricularia growing in cloud forests
with traps buried below damp moss.
Sunny epiphytic perches are more likely
to support ant-fed plants than carnivores,
due to reduced rates of evaporation
in the swollen internal chambers of theses ant-fed plants
via the, versus, pardon me,
the active secretion
of nectar and digestive fluids in most carnivores.
Indeed, almost all 300 species
of ant-fed plants are epiphytes.
Next, optimal investment in carnivory,
at least in terrestrials, should increase
toward the sunniest, moistest, and most nutrient-poor sites.
Perhaps the most striking confirmation of this prediction
is the cline in the relative size
of the photosynthetic keel versus the
carnivorous tube of Sarracenia purpurea,
the common pitcher plant in New England.
As shown here across 26 bogs,
keel size increased with the concentration of ammonium
in soil water in these natural bogs,
excluding two other sites where nitrogen
was not a limiting nutrient.
In a bog remote from industrial areas,
plants sprayed with different amounts
of ammonium nitrate showed a similar pattern.
As you can see on the bottom.
Pitchers in another bog that received direct doses
of both N and P also showed a shift to larger keels
with increasing nitrogen.
As expected, more keel-rich pitchers
had higher photosynthetic rates.
Patterns of seasonal heterophylly,
producing different kinds of leaves,
also support our predictions.
Most carnivores do not produce trap, or produce leaves
with a low allocation to carnivory,
during unfavorable seasons when moisture,
or temperature, or light might limit growth,
as seen in the pitcher plants, Cephalotus,
the Venus flytrap, and a number of other groups.
Optimal trap mechanism and form should depend on tradeoffs
associated with environmental conditions,
with prey type, and trap type.
That makes, I think, qualitative sense.
Studies on Nepenthes over the past decade
provide compelling illustrations of this idea.
Most Nepenthes grow in forest openings
over highly infertile soils and they prey on insects.
Both climate and prey type appear to shape the pitchers
of these species, and it turns out
that waxy traps with narrow cylindrical pitchers,
narrow apertures, mostly grow in the seasonally dry lowlands,
and they capture creeping insects,
while traps with wide apertures,
and large peristomes that are slippery when wet
and have a sticky or viscous
trap fluids.
The trap fluid itself is a bit of a trap.
Dominate in constantly wet forests,
usually at higher elevations,
and mainly capture ants or flying prey.
Nepenthes is one of five genera of pitcher plants
that feed to a very large degree only on ants.
This has always struck as odd.
Ants are famously successful in localizing enemies,
and food sources via scouts, who then return to the nest,
and recruit workers and bring the whole ant nation
down to deal with either.
Yet ants, I know from watching all these plants,
avidly visit each of these green anteaters.
So, what gives?
One possibility, according to Ulrike Bauer,
plant biomechanics expert extraordinaire,
is that many species of Nepenthes have outwitted
those smarty ants by having peristomes, or pitcher rims,
that are slippery only when they are wet.
Most pitchers, including Nepenthes,
have a zone of waxy crystals below the pitcher opening
and nectaries that attract prey;
and these crystals readily detach,
causing insects to lose their footing,
and it turns out,
the broken off scales contaminate the adhesive structure
on the feet of the insects;
again, causing them to lose their grip
and to slide on other surfaces.
As a result, on these plants,
the insects slip and fall into the abyss,
under all circumstances.
But Bauer has shown that several Nepenthes
have highly specialized peristomes
that give good traction when wet,
but become incredibly slippery to insects when, pardon me.
Good traction when dry, they become incredibly slippery when wet.
And then it turns out that the ridges and grooves,
you can see at different scales here,
keep water on the peristome surface via surface tension,
and they prevent the tarsi of the insects
from contacting the plant surface,
and so the prey just aquaplane into the drink.
(audience laughing)
During dry weather,
the peristomes allow scouts to locate pitchers,
and their nectaries and survive, return to the nest,
and recruit large numbers of workers to the food source.
If conditions remain dry, the ants make hay.
But as you can see if things go misty,
oopsy-daisy, columns of workers slide into the tank.
So these traps, active only part time,
which at first seems inefficient
and unlikely to be favored by natural selection,
might actually provide plants
with bonanzas based on a crucial weakness
in the social behavior of their prey.
Truly a bait and switch worthy of unsavory politicians
(audience laughing) by these green Machiavellis.
It turns out, by the way, by hooking up electrodes
to these plants, Bauer was able to show
that as the film of water on the peristome
increases in thickness, the prey capture rate goes up,
so it's high in the morning, in the afternoon,
when the humidity is high or after rain storms.
She has also found a remarkable strategy,
another way of preying in the rain
in Nepenthes rafflesiana, shown here.
Its pitchers have lids with waxy crystals
on their undersides that reduce traction
that allow insects to crawl safely under most conditions.
But when it begins to rain,
some of the ants and flies will seek shelter under the lid,
under that little umbrella,
and when the raindrops strike the lid,
it bends down and then recoils, (audience laughing)
and the insect is precipitated into the abyss.
These movements are much faster than the Venus flytrap,
require no energetic input from the plant,
and essentially use rain
and the prey's own inertia against it.
Basically, these are crafty
jiu-jitsu warriors. (audience laughing)
Now three Nepenthes species with giant pitchers
at high elevations have evolved into latrines,
and depend on the feces of tree shrews for nitrogen.
Apparently these tree shrews are all males,
because they always leave the lids up!
(audience laughing)
These three species at low elevation,
tolerate substantial shade,
apparently because they have greatly reduced secretions
of nectar and tank fluid,
and capture nitrogen either by acting as bat roosts,
in this Nepenthes hemsleyana,
or capturing leaf litter, in Nepenthes ampullaria.
Nepenthes bicalcarata though beats all.
It tolerates shade by having very long-lived pitchers.
These are kept functional by ants
that they house in little swellings on their tendrils.
You see that little twist next to the tank,
the pitcher of the plant.
And these butler ants,
basically keep the peristome clean of fungi and algae,
and, we know from experiments that have been conducted
by Clark and others that
the presence of the ants triples the amount
of nitrogen input to the leaves as a consequence,
and it's particular effective on older leaves.
Uniquely, these commensal ants can swim
in the pitcher fluid, it sort of makes sense.
They're constantly cruising the peristome
which gets slippery when wet so they're going to slide in,
but they evolved the ability to swim and then get back,
pull themselves out of the pool.
And often they will eat mosquito larvae
living inside the pitcher, and in so doing,
they prevent some of the food,
taking up by the plant from leaving the plant
and flying off with the adult mosquitoes.
These ants of course will defecate into the tank fluid.
Now Darwin suggested that snap traps in Dionaea,
the Venus flytrap, with rapid closure,
escape of small prey via spacing of marginal teeth
and digestion in an enclosed chamber,
may have arisen to capture larger,
and more rewarding prey that could be immobilized
in the sticky traps ancestral to sundew family.
Here at Maddison, Tom Gibson and Don Waller,
have developed a model supporting
several aspects Darwin's ideas,
and highlighting how important for the growth of Venus flytrap
prey capture early in its lifespan is.
Mutualistic interactions between ant prey,
and pitcher plants may further affect
and favor the carnivorous habit.
Daniel, Joel and I, a number of years ago,
independently proposed that pitcher plants
in Cephalotus, Nepenthes, and Sarracenia,
all of which prey primarily on ants,
may actually be mutualists with their prey.
Well, that's easy to say if you're the plant.
What's the advantage to the animal?
Well, look, plants in nutrient-poor habitats are long on carbohydrates.
They're photosynthetic for God's sake,
but short on N and P, and other mineral nutrients,
whereas ants in the same environment
may be relatively long on nutrients,
because of their predation on insects,
but short on energy, on carbon.
Given the large amount of nectar provided
by these pitcher plants that are specialized by ants,
and a few individuals from colonies we observe
actually being lost to pitchers,
it might pay ant colonies to sacrifice the occasional sister
into the well for all the sugar gained,
just as it might pay the plants to provide ants with large amounts of sugar,
if they gain enough nutrients, thereby,
to elevate photosynthesis by a greater amount.
Now Moon et al. have recently demonstrated that...
one...
North American pitcher plant, Sarracenia minor,
earns a net benefit from its interactions with ants.
The question remains whether a net benefit
also accrues to the ants.
If ant specialists like Sarracenia minor shown here
are mutualists with their prey,
it could generate a positive feedback
between the potential benefits of carnivory
and increasing prey density,
with the abundance of each growing larger and larger
until they eat Sheboygan.
(audience laughing)
Carnivorous plants should have lower photosynthetic rates,
and relative growth rates.
The advantage of carnivory does not lie
in absolutely high photosynthetic rates,
but simply in increasing those rates minus the costs.
A meta-analysis by Ellison and Adamec
appear to confirm these predictions
for terrestrial carnivores,
but there's a deep problem with these data:
The non-carnivores analyzed often grew on rich soils
while the carnivores grew on poor soils.
And so this study really should be redone,
if you're interested, call me. (audience laughing)
Astoundingly, no experiments
have yet compared growth and carbon uptake
by non-carnivores, and fed versus unfed carnivores
under field conditions or competitive interactions
among the plants.
I hope to pursue such an experiment in the near future,
and if you're interested in helping conduct that study,
again please see me after the talk!
Just a few last points here:
Possession of defensive glandular hairs
should facilitate the evolution of carnivory.
The pre-existence and the co-use of such hairs
would reduce the cost curve and, consequently,
reduce the energetic threshold for carnivory.
In accord with one of Darwin's proposed paths to carnivory,
five of the 10 carnivorous clades appear derived
from ancestors with glandular leaves,
as exemplified here by the non-carnivores
to the left of the red line,
Plumbago, Frankenia, and Tamarix,
their sister to the carnivorous clade of Nepenthales.
Selection for carnivory should increase if sticky traps
also continue to protect carnivores from herbivores.
Field removal of secretory glands
from this Mexican butterwort,
show that glandless plants sustain 18 times more damage
due to insects than the controls.
"Vengeance shall be mine!" sayeth the insects. (audience laughing)
Increased ant visitation to Sarracenia minor
reduces herbivory and pitcher mortality
independent of ant capture.
So, remnants of defenses against insect herbivory,
from which carnivory is thought often to have evolved,
may play an important role in maintaining selection
for the carnivorous habit.
Now anoxic or toxic soils should favor carnivory,
and replacement of roots by trap leaves on open moist sites.
Such conditions render root function costly,
and favor shifting part or all nutrient uptake
to trap leaves aboveground.
The widespread occurrence of carnivores on sodden soils,
and their small, shallow root systems,
support this hypothesis, as does the restriction
to heavy metal-rich, serpentine soils of Darlingtonia,
several species of Nepenthes,
and few species of Pinguicula and Drosera.
But, assessing the significance of shifts
from root to trap allocation using our original model
would ignore the complex interplay of allocation
to the leaves, roots, and traps
and their impacts on whole-plant growth.
And so my colleagues and I have recently developed
a new, two-dimensional model to explore these trade-offs.
It predicts increased allocation
to traps versus roots on sites.
The more inefficient roots are for nutrient capture
and the greater the response of photosynthesis to nutrient supply.
The key role, however, of roots in absorbing water
favors a mixed trap-and-root strategy,
even when carnivory is favored.
Next, growth co-limitation by multiple nutrients
may favor increased root allocation
after prey capture.
This hypothesis would seem to provide
the only plausible explanation
for this repeatedly observed paradoxical behavior
that as some carnivorous plants catch more prey,
they allocate more roots.
If two or more nutrients co-limit plant growth,
then prey capture elevates the level of one nutrient,
increased root growth should be favored as a means
of getting the other nutrient below ground.
Adamec has argued
that prey are such rich sources of nitrogen and phosphorus,
and such poor sources of potassium and magnesium,
the prey capture might favor increased root growth
to retrieve potassium and magnesium.
Last couple of points.
Paradoxically, bladderworts in harder,
more fertile waters should invest more in carnivory.
Well, how can that be?
Well, it turns out that harder waters contain more cations,
and often more phosphorus and nitrogen,
but they also contain more CO2 and more carbonate ions
from which additional CO2 can emerge
as photosynthesis proceeds.
The greater the concentration of CO2 and bicarbonate,
the more photosynthesis should be enhanced
by a given increment of prey capture,
favoring greater trap allocation
in those harder but more fertile waters.
Indeed, Susan Knight,
working here at the University of Wisconsin long ago,
found that trap number in bladderworts
in Northern Wisconsin lakes increases with water hardness
and the fraction of biomass allocated to traps
in Utricularia in Czech lakes increases
with the amount of dissolved CO2.
Adamec has shown that, in laboratory conditions,
addition of CO2 greatly increases allocation to traps,
while addition of prey only slightly increases trap allocation,
and both of these are consistent with the predictions of our model.
Finally, anoxic or infertile soils select
against the evolution of tall woody carnivores.
The almost complete restriction
of carnivory to relatively short herbs is remarkable.
And again Darwin did not explain that.
Wet, infertile soils are favorable for carnivory
but work against tall, woody plants of any kind
because of their lack of, or channels in the roots
and the ease of toppling such trees in wet soils.
So I suspect that no matter how widely
we explore the Earth for new carnivorous plants,
(audience laughing) we need never fear
an Audrey II scenario! (audience laughing)
To conclude, many of the assumptions and predictions of the cost/benefit model
for the ecology and evolution of carnivorous plants,
in its original and new forms, appear to be supported.
The most powerful tests of our models in the future
would entail making them fully quantitative
and then comparing quantitative predictions
of optimal plant form and physiology with reality.
In addition, field experiments
on the growth and competitive ability
of carnivorous plants versus non-carnivores
in different contexts would be extremely helpful.
The revolution in our understanding of carnivorous plants
is likely to continue as new genomic data
allow us to fully understand the development
and operation of the traps, assess selection on them
in different environments, and quantify the impact
that carnivory has on nutrient acquisition, photosynthesis,
whole-plant growth, and competitive ability.
Only then will we fully understand
these most wonderful plants,
which have ensnared our attention ever since Darwin.
Thank you very much.
(audience applauding)