SPEAKER 1: So with those words of praise, I give you Professor Robert Raguso speaking about "Whispering Willows and Lying Lilies. "
ROBERT RAGUSO: Thank you, John. And thanks to Sonia and the Plantations for the invitation to speak with you tonight. I want to especially send a warm thanks to the class of 1945 with whom I shared dinner. Thank you for welcoming me to your mini-reunion. It was a very inspiring evening.
I have a strange challenge tonight because this is a different audience than I'm used to teaching to. And what I'd like to do is what I do with my students, which is I like to show data. I like to show-- don't worry, (LAUGHING). Eyelids are already beginning to go half-mast.
No, when we talk in our classrooms about what we know and why we think we know it, I like to show the evidence. I like to show my students where those inferences come from. And so you can take out of tonight's presentation what you'd like to take out of it.
There's some chemistry. Beware. But chemistry is the language of plant/insect interaction, just as mathematics is the language of physics and biochemistry and, in fact, biology too.
And what I will be careful to do is make sure to walk you through slides where I think it might be a little technical. Or it'll just be valuable to give you an extra moment of description.
Now, when we talk about plant behavior, most people think it's a joke. Or they think of Little Shop of Horrors. Or since we're talking about our children's influences on us, my son is 13, and he plays "Plants and Zombies" on his computer. So in his mind that's what plants do. They shoot peas at zombies.
Or we think of the kind of plants that really fascinated Charles Darwin and other scientists of his generation-- carnivorous plants, sensitive mimosa, plants that do move in the human time scale. But that's not really what this evening's talk is about.
I'd like you to take a moment to just look at this image. Welcome, the class of '45 back to this beautiful campus. We've had a gorgeous autumn. So just let your eyes cast across Cayuga Lake to the far shore and look at the trees. And just let your mind wander and free associate what the words are that come to your mind when you see those trees.
If one of the words that crossed your mind was scenery, raise your hand. No, no, you're not being honest with me. Well, that didn't work because it's been my perception for most of my adult life that plants, to 9 out of 10 Americans at least, are scenery.
They're passive background. They're not the life support system of the planet. They're not active participants in their own biology. They're not dynamic, vibrant organisms. They're scenery. And so the rest of my presentation is about how that's not true.
Despite the persistent idea that plants are passive, there is a subtle meme making its way through Western civilization at least about the peril of taking trees for granted. We can begin with Shakespeare. In Macbeth, Act Four, some of you will remember that that Macbeth is starting to feel a little worried about his strategy and what might happen to him. And he goes to see some witches to ask if they can foretell the future.
And we pick up in Act Four, Scene One-- the third apparition shows up and says, "Macbeth shall never be vanquished until Great Birnam Wood to hide Dunsinane Hill shall come against him." Well, Macbeth laughs and says, OK, great. That'll never be. Who can impress the forest to bid the tree to unfix his earthbound roots?
And he goes on to kind of boast about how his job is secure in Dunsinane. And as the sunrises over the hill, and, in fact, Birnam Wood is looking like it's coming to visit Dunsinane. And we know that it ends very badly for Macbeth. (LAUGHING) So that's part one of revenge of the trees.
Part two is picked up right after the war by JRR Tolkien and dramatized so lovingly in Peter Jackson's movies in the last decade. So here is Treebeard, the Ent, walking with the hobbits Merry and Pippin and rousing the other Ents to march upon Isengard to the wizard Saruman, who has betrayed nature by burning Fangorn Forest in order to create his engine of war.
And he says, "Of course, it is likely enough my friends that we are going to our doom, the last march of the Ents. But if we stayed at home and did nothing, doom would find us anyway, sooner or later. That thought has long been growing in our hearts, and that is why we are marching now. It is not a hasty resolve. Now at least, the last march of the Ents may be worth a song."
And in fact, as is often the case with Tolkien, there is a song that bursts out. "Though Isengard be strong and hard, as cold as stone and bare as bone, we go, we go, we go to war to hew the stone and break the door."
And in fact, things ended very badly for Saruman at the end of that scene. So wizards and kings ignore trees at their peril.
Which brings us to a modern day wizard, David Attenborough. We who work in primary research are active in leading our students and our postdocs into the field to study new things, frequently derive what we think-- we like to think that we offer a lot to popularizers of science because we are producing science. And there is no better popularizer of science, at least in the biological sciences in my lifetime, than David Attenborough.
And so to give credit where it's due, one of the points I want to begin with tonight is that we doing research often derive great benefit from very talented popularizers of science. I have grown up with David Attenborough's videos. And The Private Life of Plants was a turning point for me as a biologist.
I was, at the time that these came out in the mid '90s, I was in the insect phase of my training. And there were two major themes that come through loud and clear in this video series.
And if any of you have not watched these, we'll watch a little bit this evening. I strongly recommend that you rent them from the library or get them for yourselves. They are beautifully made.
One theme is that plants possess as much agency in their survivorship and reproductive fate as animals do. They simply operate at very slow time scales. So this is the reference by Treebeard to being hasty. OK, trees are not hasty. Most plants are not hasty. But that doesn't mean they're not changing and moving and responding to their environment and, in fact, manipulating it.
But also, plants are sessile. That means they can't get up and move in most cases. So like coral reefs they're rooted to the ground. And that means that they have to use more devious mechanisms to manipulate other organisms to achieve their ends or to use the natural world-- wind and water and currents-- to satisfy their goals.
The other great influence on my thinking as a young scientist, as a young professor, came out at the end of the 1900s and early 2000s. Michael Pollan wrote this gorgeous book The Botany of Desire. And he takes this idea a little bit further that not only are plants manipulating animals, but they're manipulating us.
So this is the idea of domestication as a dialectic-- that the last scene in The Life of Plants is David Attenborough walking through a corn field or a wheat field and ruminating on the idea that wheat isn't from Kansas, you know, and corn isn't endemic to southern Africa. But through the process of domestication, those plants have used us to move them around the world. And their reproductive biology is doing pretty well.
And so what Michael Pollan does, for those of you who haven't read the book, is he explores four different themes, four different kinds of human desires-- desire for beauty, desire for sweetness and flavor, desire for alternate experiences, and desire for control over food. And he talks about how tulips, cannabis plants, apples, and potatoes have shaped human history and have domesticated us. And, in fact, I think most historians and archaeologists agree that there really isn't any human history written before we domesticated plants and they domesticated us.
So it's a very thought-provoking book. It comes before The Omnivore's Dilemma. But to me, it was an extremely thought-provoking book, and I teach with it. So I want to give credit where it's due before I plunge into the parade of ideas that constitute the rest of my presentation.
So here's where we're going tonight. This is our outline. The question I'm really asking is not only do plants behave, but how. How do they show active agency in their survival and reproduction?
I'm going to begin by giving you a little overview of plant politics. And what I mean by that, and this is borrowing from David Attenborough, is what do plants have to behave about? Who do they interact with? Who are the players in their world? And what are the themes?
After that overview, I'm going to talk a little bit about the whispering willows part which is really about plant defense against their enemies, which includes communicating with each other, which they do.
And then finally, I'll end with the lying lilies, which is my field-- pollination biology. And not all of them lie, but I'll be talking a little bit about how plants communicate, how they court each other through the Cyrano de Bergeracs of the pollination world. That's what they have to do. They need a third party. And the way they do that is endlessly fascinating for me and my students, some of whom are here in the audience, in fact.
So let's begin by reading the tea leaves. If trees could talk, what would they say and to whom? There are three themes that pop up from what I'm going to show you. One is signaling to their partners.
So trees don't grow in a vacuum, and we're talking about herbs as well as trees today. So plants don't grow in a vacuum. They are embedded in a complex matrix of their communities-- other plants, microbes, all kinds of animals, fungi, bacteria, et cetera.
And they need to communicate with each other about who's who and what they're doing. And so when I talk about keys and secret handshakes and code words and personal identification numbers, that's all chemistry. And I'll show you some of that tonight, but almost all of those dialogues are about special chemical signals and the ability to read them and respond to them.
Second category-- signals within and between plants, the neighborhood effects of alarms. Plants respond slowly to their environment, but they do respond. And they respond in ways that can be perceived by other organisms around them.
The idea of signaling within yourself, self-communication, is a very unusual idea. It's a very small theme in the study of animal behavior. But for plants, that could be as large as kelp or giant redwoods or a grove of banyan trees, communicating with yourself is not trivial.
Then, finally, eavesdropping by parasitic plants, going on the offensive. So the idea that you might benefit from perceiving what your neighbors are experiencing, which we all do. We're very social creatures. That could be turned on its end by an individual or a species that exploits that information to its advantage.
Every kind of organism in the world, every class of organism in the world, includes exploiters or cheaters or parasites. And plants are no exception. By that I mean not only parasitic plants that have no chlorophyll and can't make sugar for themselves through the use of sunlight and carbon dioxide but also plants that use other plants or trees for structural support-- vines, lianas, et cetera. So we will talk a little about that too.
So let's begin with a little diagram that's just a placeholder for me to talk about a few of the players. This is from a review paper about microbes, but it could really stand for everything.
A lot of plant biology until maybe 10 years ago was dominated by what's above the ground. So one of the current revolutions in plant sciences across the board, from molecular genetics to community ecology, is about what's going on down here.
And I'm going to collectively refer to this zone as the rhizosphere. We have atmospheres and tropospheres and biospheres. This is the rhizosphere. And that simply means the collection of microorganisms and macro organisms and soil chemistry and nutrients that's all very dynamically and actively interacting down here below ground where we can't see it.
But what you would see, if this were a better slide, is that there's all kinds of fungi and bacteria and viruses that could assault a plant above ground. But below ground, there's is a really interesting mix of things. Again, there are pathogens. There are disease organisms. Some of them are multi-cellular. Some of them are single cellular.
Some of them are fungi that live within roots-- so mycorrhizae, a very important group of fungi that have a very ancient record to the extent that we can find fossils with them, we suspect, as biologists, that plants couldn't really make the transition to living on dry land without them-- without the exchange of nutrients that takes place and the increase in surface area. Nitrogen-fixing bacteria-- not all plants have them, but certainly legumes and alders do. There are many ways to do that.
And so there's all kinds of partners down here. Some of them are positive in their net outcome. Some of them are negative or antagonistic. Some of them are neutral, or their effects are conditional, depending on drought or nitrogen or phosphorus or whatever. I want to leave you with the idea that's a very active world. So that's a single plant.
Another thing to keep in mind for today is how plants are built, how plants are made. So this is nice slide from about 15 years ago showing what happens when you put green fluorescent protein into a gene and then let that express itself in a tobacco plant. This is, in fact, from jellyfish.
So this is a very nice example of how in research we never know where a really good idea is going to come from. And if we only focus on two or three kinds of organisms because we have their genomes and we think we know everything about them, we're not going to make leaps of utility like putting jellyfish genes into tobacco plants that allow us to light up the vascular system of those plants and look at all the xylem and phloem vessels that unite the different chutes and roots and leaves of this plant and allow communication between the different parts.
What you see on the right-hand side is-- this is an old paper. This is a 17-year-old paper by a real giant in the field, Bud Ryan. And what he's showing here in this little slide, this is a photograph, sorry, with carbon 14-labeled sugar and a little peptide that's involved in plant response to stress.
And what you see here is a time course-- that there was a nick made in the leaf, and then the sugar or the systemin was added to the leaf. And what this group is doing is they're just looking at how long does it take that labeled substance to move down the axis into the chute and down the chute to a node and eventually down to the roots. It takes hours. It takes a very long time.
So on the theme of not being hasty, if a plant had to respond to an urgent attack-- a large animal, an elk or something, chewing on it-- it couldn't respond very quickly using a diffusible signal that's moving through the vasculature of the plant. So remember that when we start talking about talking trees, that using volatiles to talk other limbs of the same plant is probably a better way of getting that message through.
All right, now the purpose of this slide is to show you that, in fact, plants don't grow in a vacuum, and they grow in communities. So here, take one of our focal plants and now look at what you have is a heterogeneous community of different kinds of plants. Some of them invest a lot more energy above ground. Some of them invest a lot more energy below ground.
And there's all kinds of interactions going on here, some of which are with volatile organic compounds, odors, some of which are with nonvolatile secretions coming off of the plant, a lot of these things exudates. A lot of them are mediated by fungi or bacteria that live in concert with the plants. So there's a real community going on here.
One of the costs of living in this kind of arrangement is that you have lots of neighbors. And you need to know when to compete with them, when to cooperate with them, and how to know your neighbor's identity.
So there's our first theme-- rule or first theme for behavior is can plants identify to some extent what their neighbor is? Is it like them? Is it unlike them? And how do they do that?
On the plus side, one of the potential benefits to having this kind of a matrix in your community is an idea that's been a little bit dramatized in the recent avatar movie. If you remember that the Tree of Souls is this great nexus of electrochemistry where all the trees on Pandora are communicating with each other underground. So it's a little bit of a funny, popular idea.
But in essence, there is some evidence now in ongoing studies about roots and rhizosphere that when you have mycorrhizal fungi that are basically forming connections between different kinds of plants, there is the potential for chemical signals to move between them, to propagate through a community in response to stress or to attack or to strong changes in climate.
So let's talk a little bit about this idea of identifying self. I won't talk too much about roots the rest of my talk because I'm not an expert on it, but these are at least interesting. In my department in neurobiology behavior, one of the famous themes of research is social biology, and in particular, kin selection.
So whether they're different kinds of rodents or mongooses, these are southern African animals. And a lot of this research focuses on when do you make warning calls? Are you more likely to make them when you're related to the animal that's closest to the predator? And how do you know that you're related to them? And so forth.
Paul Sherman and a lot of his students over the years, several other people in my department, have made their reputations in some ways as scientists by studying these kinds of animals and the evolutionary selective pressures that lead them to distinguish between kin and non-kin.
So we might predict that in dense stands-- lots of plants grow in clonal stands. Many of you know this-- the goldenrod and quaking aspen. When you see an individual tree, so to speak, above ground, that's what we call a ramet but not a genet. It's not a genetically different individual. Many of these are genetically identical, and they're sharing an underground communication system. So the genetic individual is this patch.
So when you're growing in that kind of a setting, you would imagine that there'd be a pretty strong selective pressure for them to know that their neighbor is self. So you predict that kin selection should reduce competition between neighbors if they can tell that their neighbor is related to them.
And so I want to show you the beginnings of a small experiment that was published a few years ago that addresses this question. Can you see this in the back? A little? Yeah? Maybe? More or less?
So what you see here are little seedlings. This is Arabidopsis. It's a small mustard plant, and it's very commonly used in research because it has a small genome and it's been sequenced. And we know a lot about what it does, that you can grow them very, very quickly so you can do a lot of experiments in a year.
What you see happening here is these are seedlings and their roots. The seedlings are being grown in exudates. So it's sort of a water bath taken from different plants' roots.
So where it says "Own," this plant is growing in its own exudate, in its own juices so to speak, in its own environment. Kin-- this plant is growing in an exudate taken from a sibling. Stranger-- this plant is growing in an exudate taken from another seedling that isn't genetically related to it.
And here that experiment is being repeated except it's being repeated in the presence of sodium orthovanadate, which you don't have to know for the test (LAUGHS), but it's a blocker. It prevents the plants from secreting phenolic compounds from their roots. So it's basically a mute. It's a silencer. If these plants are communicating with each other through phenolic secretions, it's not going to happen with sodium orthovanadate.
So what happened in the experiment was this. In the absence of the blocker, the plants produced more lateral roots, which is always interpreted as a competitive response, in the presence of exudate from an unrelated plant. Whereas, there's no difference statistically in the number and length of the lateral roots growing in its own juices or that of its brother or sister.
So this is not an overwhelming result, but statistically it suggests that these plants are capable of identifying each other through the root exudates. And when you block that ability to exude phenolic compounds, there is no response here. There's no difference between any of these three treatments.
So there's a lot of results like this in the literature. And they're beginning to accumulate in different kinds of plants-- wheat, annuals, perennials, et cetera. But these are the kind of things that people are beginning to find.
Eavesdropping. Sometimes you grow next to a plant that isn't related to you. What you see here is a photograph taken from the Great Basin in Utah and Nevada. It's a high, cold desert dominated by sagebrush-- artemisia tridentata. It's a magnificent plant. It smells divine. In fact, the odor of that plant is the smell of the Great Basin.
And, of course, it's from a group of plants that is medicinally very important. They're called the wormwoods because of their utility in treating parasitic diseases of different kinds of helminth worms in humans.
And what you see growing next to it are little, weedy tobaccos. These are annual plants. They don't live very long. And these plants have been studied by Ian Baldwin and his students now for about 20 years.
And what you see here is a diagram of what they think is happening. The plants that live closest to the sage brushes are capable of perceiving when the sagebrush is under attack because it produces these different volatile compounds. And these plants respond to it by ramping up their production of defense compounds and toxins to protect themselves.
That works for about 15 centimeters, so if they're neighbors, it works. Most of the data show that if you're really far downwind, this doesn't work very well. But these are at least the first kind of data from the field-- not only by Ian Baldwin but by also by Rick Karban at Davis-- showing similar things.
So I want to give you just a brief history of the whole talking trees field-- where did it start, where did it go, and how does it get us to tonight's talk. It started really in the early '80s. So we're running on 30 years now since people really began to ask plants if they could communicate with each other.
David Rhodes of the University of Washington did an experiment where wounded plants and their neighbors resisted subsequent attack, so there was some suggestion that the exposure to the wounding compounds allowed the plant to ramp up his defenses.
Ian Baldwin, as an undergraduate at Dartmouth working with Jack Schultz at the time, did a really classic experiment, in fact two classic experiments published in Science-- one with oak trees and one with poplars. They didn't want the rhizosphere to be responsible, so they put the plants in pots.
And what they found was that potted trees increase their defenses, in this case tannins, when they're downwind from plants that had been wounded using gypsy moth caterpillars. And this provoked a firestorm. The responses to it-- they made it into cartoons. There were all kinds of political satire made in response to this paper. It really touched a nerve.
And I think what was unfortunate was at the time the technology wasn't available to really ask what are the signals? So the field kind of puttered along until the early '90s when Bud Ryan and his students did the first classic experiment clipping sagebrush and looking at what happens to tomato roots.
Now, they were working in Washington state in Pullman, Washington, which is just on the northern edge of the Great Basin. And this experiment started as a mistake that one of the vents was open, and it was sucking air from damaged sagebrush into the greenhouse where Ryan's tomato plants were growing. So this is like the discovery of penicillin.
And when Ryan and his student did assays of the defense compounds in the tomato plants, the ones near the vent were off the chart. And they said, wow, what's going on with the vent? And they realized that the sagebrush was part of that.
As I told you, Rick Karban went out into the desert and asked if tobacco plants can eavesdrop on sagebrush. The criticisms at the time were that there were too many alternative hypothesis that hadn't been dealt with. Plant communication was such a heretical idea that people wanted to see other hypotheses eliminated first.
The wound odors are, in fact, dilute. And outside of the greenhouse area, when you're in the Great Basin and the wind is howling, it really is an open question as to whether you have enough of a concentration of odor to really make an impact on a neighboring plant.
And then finally, while there's obvious selective advantages to be listening for other plants, there's not necessarily an obvious reason why you should be sharing your secrets if you're the wounded plant.
So that's where the whole idea of plants talking to themselves came from-- that if plants aren't really intending to broadcast the fact that they're wounded or under attack, maybe that's just an epiphenomenon, or a byproduct, of the fact that plants are large and that the vasculature is slow. And the way that they respond to being damaged is to puff odor to the other parts of the plant so the whole plant systemically can ramp up its defenses within two or three hours instead of days.
That brings us to part two which is really about the concept of priming. So here's a tomato plant being chewed on by a tobacco hornworm caterpillar. These are the animals we study in my lab. They grow up to be excellent moths. They can decimate tomato plants as many of you know from your gardens.
And so what happens is when they cause wounding damage in a leaf, that creates, initiates, a vascular signal that moves slowly up the plant and down into the roots, and it's mediated by this compound jasmonic acid-- not on the test. You don't have to know it.
But it's a phytohormone. It's a molecule that has a really specific set of functions in all plants, in fact. So it must be very ancient.
But it also produces volatile, airborne molecules. So this is the methyl ester of jasmonic acid. So there's a methyl group here over the alcohol.
And for the chemist in the group, that makes it volatile because the possibility of hydrogen bonding to a sugar is no longer there. So this can move quickly outside the plant and be perceived by leaves across the plant.
And those compounds initiate a cascade of odor production. What happens is that the cell membrane of the plant leaves begins to degrade really quickly into a whole set of compounds that smell like freshly-mowed lawn grass or really green, unripe apples. You know that smell? It's just the smell of a grass stain on the pants of an active child. And those compounds have all kinds of functions that we'll talk about.
What's really magic about this is that the thing that triggers it is spit from the caterpillar. If you take a scissors and cut those leaves, you'll produce some of these odors, these freshly-mowed grass odors just as you do with your lawn mower. But it's not going to make the whole plant five hours hence start smelling like a Jasmine flower.
But if you cut one of these leaves with scissors and then rub saliva from a caterpillar into it-- if you do those kind of things-- [LAUGHTER] you'll find that amazing things happen.
So here, this is the molecule. And again, for the chemists in the group, this is a special molecule because it's a chimera. Half of the molecule is a fatty acid byproduct coming from the chopped-up plant. The other half is an amino acid coming from the gut of the caterpillar.
And they are conjugating into a chimeric molecule. And that molecule is the trigger that turns on all of this.
And what's really special is that if it's a different caterpillar, it's a different molecule. So there's where the personal identification numbers start coming into play. So point number two, plants know not only who their neighbors are by the phenolic exudates of the roots, but they know who's eating them by their spit.
And that's important because the defense compounds that the plant needs to marshal to get rid of these guys are different than the ones that they need to marshal to get rid of other kinds of biting insects. And the fact that plants can do that is one of the most amazing discoveries of the last decade.
But that's not all, because plants have other enemies. The microbial enemies do things like this. Many of you have seen this in your gardens. This is what we call a hypersensitive response. So a virus or a bacteria or a little fungus is attacking the plant. The plant is circling the wagons and trying to limit the damage. Usually that's a peroxide response that the cells around the point of damage are flooded with hydrogen peroxide. And then there's a wall built, literally, around them.
That process is mediated by a completely different plant hormone-- salicylic acid. Now, here's where the willows come into play. Salicylic acid is named after salix, the Latin name for willow. It was discovered in willows. And then if you know what salicylic acid is related to, it's related to aspirin.
But here's the rub, salicylic acid, like jasmonic acid, is not volatile. It's often linked to sugars. It's very valuable in plants. It's used for a lot of different things.
It can diffuse slowly up the vasculature, but it's methyl ester is volatile. And that can diffuse in the air immediately over the entire plant and really ramp up the systemic response of the plant, not having to wait five hours or 10 hours for the salicylic acid signal itself to get there.
What's so interesting about aspirin, from a plant point of view, is that the salicylic acid response and the jasmonic acid response are antagonistic to each other. That's something that we call cross-talk. And my friend and colleague, Jennifer Thaler in entomology, is one of the world's experts on cross-talk and what are the subtle interactions between these two ways that plants have of defending themselves against different kinds of enemies.
Many of you know that if you add a tablet of aspirin to a vase of cut flowers, they'll last longer, right? They won't senesce. The reason for that is that salicylic acid and its acetic ester, if you will, they block jasmonic acid signaling, and that blocks ethylene.
Ethylene is a very small molecule that's very important in plants because it's responsible for about 1,000 different processes related to decay, death, and degradation-- senescence. So the plants don't senesce if they can't perceive ethylene. And they can't perceive ethylene if you've got aspirin. And that's a very, very ancient interaction.
Aspirin is useful to us because it blocks prostaglandin biosynthesis at the point of swelling in our bodies. And prostaglandins chemically look just like that. So there you go.
Now, I want to segue to something called indirect defense. Direct defenses are obvious. Plants have thorns. They're filled with toxins. They have grown and are ready to defend themselves. In fact, in some cases they advertise their suitability to defend themselves, like porcupine's do. I mean, a cactus is nothing if not armed to the teeth.
But those things have costs. If you invest a lot of nitrogen and carbon in defending yourselves and making heavy toxins and making really complicated molecules that kill other animals or in making spines, that's energy that, in theory, is not available for your growth and flowering and fruiting and seed production. So what if you could actually hold back a little until it was dangerous and you knew that you were going to get attacked? Could a plant do that?
Well, that's what an indirect defense is through induction. And there's two major ways that plants do this. One is by calling in the cavalry.
The method that I just showed you-- here is a caterpillar eating a leaf. The spit factor of allicin is produced. And that whole cascade results in the emission from the whole plant a very sweet-smelling odors that are attractive to carnivorous insects. This includes parasitic wasps, who want to lay their eggs in the caterpillar, and also hunting wasps that want to eat the caterpillar or bring the caterpillar back to their nests and feed them directly to their young. So one way or another, they're feeding their young with these caterpillars.
And this has been demonstrated in several systems-- cotton, corn, tobacco-- to function quite beautifully. So you have a mobile army of parasites or carnivores and you feed them and their offspring.
The other way to do this is to house the army yourself. And around the world, there are several different evolutionary origins of so-called ant plants, plants that keep a standing army of ants, or even mites, living on them as predators. They give them a place to live-- a hollow thorn. They give them food to eat for their young. These Beltian bodies on an Acacia tree are full of protein and lipid. They give them sugar and sugar and more sugar. These are called extrafloral nectaries because they're at the base of the petiole of the leaf. There's no flower there, but they're gushing nectar. And then the ants are addicted to it.
So one of the ways that these plants can respond to imminent danger is that if they are getting attacked, they can actually ramp up the sugar level, and that usually really sets the ants rolling, even if they're already living on the plant.
Let me show you an example of a really nice study that demonstrated how this works. This was done by a friend of mine named Martin Heil in Mexico on wild lima beans. And wild lima beans, when they're not in a garden, are kind of sprawling vines. They could be meters and meters long, and branches that ramify into all kinds of host plants that they're sprawled over. So again, communicating within a lima bean plant is not easy.
What you see here is two branches from the same plant. Here's the lima bean plant. This one has a bag over it. And the leaves inside the bag are being exposed to volatile compounds, odors, being produced by the wounded part of the plant.
This is a chromatogram. I'm going to show you several of these in the talk. Don't be afraid of them. This is just simply a graph over time. And each peak is an odor being separated by its boiling point in a relatively simple oven-like machine that we use all the time.
When the plant isn't being attacked, it doesn't smell very much. When it's under attack, it produces all these wounding compounds elicited by the process that I just described to you. And it smells strong and sweet.
When you expose those odors to undamaged leaves inside of a bag, here's what happens. Over the span of a few weeks, the leaves that were exposed to the volatiles suffer less damage by enemies, by herbivores, by chewing insects, than the ones that were left out in the open. And conversely, they show more growth. They have more living tips present on them at the end of the season than the ones that were left open. So there's a definite survivorship advantage to the leaves or branches on this plant that were exposed to these odors.
And the question is, how does that work in lima bean? I mean, anybody can measure these results, but knowing the mechanism is not so easy.
Well, what they did was they repeated the experiment at a finer scale-- same branch, choosing to bag individual compound leaves and expose them either to the odor blend of a wounded plant or to the odors of a non-wounded plant.
What they found was that the plants actually have extrafloral nectaries at the axles of the leaflets. So like the Acacia, they can attract ants by gushing sugar. And what this graph shows you is that for leaves one through three, they didn't make any more nectar than they would have if they were not exposed to the volatiles.
For the leaves that were in the bag and were being exposed to these odors, they really ramped up their nectar production. It was kind of a threefold increase of nectar from these little nectaries. And then the ones at the tip that weren't exposed, again, they didn't do anything.
So here's the mechanism-- that lima beans can scream for help when they're getting attacked if they're exposed to the odors of their own wounds. And the way they do that is by producing more sugar and bringing ants. The ants are already there walking around looking for sugar, but when they find it, they stay.
So I talked about eavesdropping, and we talked so far about when eavesdropping should be something that you do to kind of help your own survival. If your neighbor is getting attacked, you can kind of prepare yourself if you're next.
What about plants that go on the offensive? This is a study that was published a few years ago from Penn State about a parasitic plant. So if you can see these little threads here.
This is called dodder, D-O-D-D-E-R. It's a parasitic plant so it doesn't make sugar. It doesn't do photosynthesis. And it's related to morning glories of all things. You wouldn't know it by looking at it because it's so reduced and miniaturized that the flowers are tiny. They just self-pollinate in the bud. You would never know.
This particular case is a dodder species that attacks tomato. And what you can see here is that the seedling germinates, it moves toward the tomato plant-- we don't know how-- grows around it, and then starts putting suckers into the tomato plant, and begin siphoning off nutrients to grow its own body. And that's how parasitic plants work.
So what the authors of this study did was they wanted to know is the dodder actually using the odor of tomato plants to find the tomato plant? When the seedling comes up out of the ground, is it basically a vegetative nose? It's snaking around. Is it finding its host that way?
Insects find their host that way. Monarch butterflies are always looking for milkweeds. And they taste. They taste the ground above the root crown. They taste the leaves. And that's how they know where to put an egg. What if the dodder did the same thing?
So what these researchers did is they made a little chamber, a light-proof chamber, where they could essentially put a dodder seedling in the middle and make it choose to go this way or that way, depending on what odors they put. And they had it at right angles so there's no possible way for reflected light. There's no blue or far red or near red. There is no light signal that could possibly reach this plant in the dark.
And what they could then do is use these rubber septa with extracts of tomato plants in solvent. You could control for the solvent, or you could put the tomato plant in there itself and blow air over it and see how does the dodder plant respond? So what you're going to see are a bunch of disks cut into north, south, east, and west quadrants and their behavioral assays, their choice experiments for seedlings. This is remarkable.
So if the top and the bottom odors are from moist soil, the seedlings shouldn't choose because there's nothing there. And in fact, they don't. So there's 16 to the top, 14 to the bottom. The distribution around the circle is not too bad. They're not really choosing here.
For a 20-day-old tomato plant down here, there is a pretty strong preference shown by the seedling to grow toward the tomato plant. So that's what we call a positive control. That shows you that the experiment works-- that the seedling is choosing to grow toward the direction it should be if it's going to find a host.
This is a rubber septum with tomato volatiles. So you can collect volatiles, or you can wash the plant with alcohol and then put that on the rubber septum and put that in here. And here's the seedlings growing toward that end. So there's something about the odor of the tomato plant that is drawing the seedling to grow toward it.
So when you've got that kind of a result, then you can start asking, well, which odor? We know what tomato is. Tomato is made up of 45 or 50 different compounds. We could start looking at which compounds might be the ones that are attractive to the seedlings.
And so here's the kind of data table you get when you do that experiment. Here's each of these compounds. And here's the number of seedlings that are choosing the half of the disk with or without the odor.
So the ones that I've highlighted in green for you, these are three compounds that are related to each other. They smell like turpentine. In other words, they smell like a tomato leaf.
And what you can see here is that there is a twofold preference of the seedling to grow toward the half of the filter paper disk that has the volatile versus the half without the volatile. In other words, they are attracted to these compounds. There's a bioassay that works.
What's really interesting is they are repelled by this one. There's a twofold preference to grow away from that compound here. And that's not a 10-carbon compound that smells like turpentine. That's the compound that you make when you wound a tomato plant.
So what's happening is this seedling of dodder is growing away from a wounded tomato plant odor. That's pretty nice. Not only do you know who you are, know who your neighbors are, know who's eating you, but you know when your host plant is sick. And you should probably not go use it because what the dodder does is it taps into that plant. You don't tap into a sick plant if you're a parasite.
One more example of this really interesting cut-lawnmower odor and that'll segue us into flowers and pollinators, and that'll be the last part of my talk. This is an orchid, and I included it today for two reasons. One, it's my segue. And the other is it's a European orchid, but it's local.
We've got this in Six Mile Creek. We've got it in several different forests around here. It's a midsummer bloomer, and the flowers are not stingy. They're full of nectar.
What's strange about this orchid-- and there is an orchid that does everything as you'll see later in the talk-- this particular orchid smells like cut grass. So it's playing a very strange game. It's being pollinated by wasps, yellow jackets and mud wasps. But these wasps respond to this odor by looking for caterpillars as I showed you.
When they get to this plant, they don't find caterpillars. They find lots and lots of sugar, and it doesn't bother them. So it's a shell game. It's a bait and switch that actually has no costs for the plant or for the pollinators because everybody's happy in the end. It's a happy ending. It's a Disney World flower, in fact.
And this is just a chemical analysis that shows you that here is where those odors are. And here's the antenna of the insect showing an action potential in response to those odors. So they don't smell everything the orchid is making. They smell the cut lawnmower odor.
And that's what gets them there. And once they get there, they learn everything else about that plant because it's the best nectar in the forest.
So I'm going to finish up now by talking about flowers since the lying orchid got us there. And flowers, for me, have been a challenge because the chemical world of flowers has been very poorly described, in general, in the history of botany because, I think, we're very visually-oriented organisms. Our language is full of visual metaphors. And the study of pollination biology from a visual standpoint goes back to the late 18th century to Springle, who was very interested in bull's eye patterns on flowers.
So this is something that my predecessor in neurobiology behavior, Tom Eisner, was very interested in. When you look at a flower with the eyes of an insect-- so you shift your color vision into ultraviolet and away from red-- what you find is that there's patterns that we don't see because we don't see ultraviolet.
This evening primrose is not uniformly golden. It has an ultraviolet-absorbing center which is insect black essentially. So these patterns often are informative because they direct, visually, an insect visiting a flower to where it would find nectar or pollen.
So here's where the botany of desire gets to be really interesting for us, why the tulip overran the economy of the Netherlands, for example. Flowers are reading our brains. They've tapped into our aesthetic sense to the point where we can't think about them as reproductive organs of plants. We think about them as things of beauty and objects of courtship for our own sexual interests, romantic interests, which means that we've often been distracted away from what's really functionally important about flowers.
Flowers that are honest-- so the first half of this section is about flowers that don't lie, are not lying lilies-- they have something to offer. They're essentially a part of a marketplace. And what they have to sell is sugar or pollen-- pollen and proteases. It's full of lipid. It's very rich.
And so typically, the odors and colors and signposts and things are about where do you get the commodity? And I want to take a few minutes to talk about a remarkable plant that I got to know in South Africa during a sabbatical trip that I took about six years ago with my family.
This is a kind of iris. It looks different than American irises, clearly. And what's so interesting about it is it looks like it has roadsigns. So if these flowers are showing with ultraviolet where to go to get the nectar, these flowers, which are pollinated by a very long-tongued fly, are showing where to put the tongue.
I want to show you a few minutes of video because you really have to see this to believe it.
- Make drinking even more difficult for their couriers. This small iris grows in South Africa. Each flower has a hugely elongated tubular base. The tiny entrance to it is indicated with exemplary clarity and absolute accuracy by these white arrows on the petals.
And here is the only tongue that can reach that nectar. It belongs to a hover fly. It's not so much a tongue as a fine tube. But in proportion to body length, it's one of the longest feeding implements in the animal kingdom.
The clear markings are particularly important because the tongue is so long that even in the lightest wind, the end blows about. An extra thrust is needed to get the last drop.
The iris only flowers for a few weeks, so what does the hover fly collect with its phenomenal tongue at other times?
ROBERT RAGUSO: OK. So that's what I saw on my belly (LAUGHING) 3,000 feet above the valley floor in South Africa. And my host, Steve Johnson, who is a really amazing botanist, went out the next year and started to do an experiment. And I want to walk you through this experiment because it's a marvel of clear thinking and low technology.
So here's our flower. And here's the pollinator. And that's my photo. I worked very hard for that photo. (LAUGHING)
And so we have a hypothesis that the Lapeirousia irises have high-contrast markings on their flowers. Do they serve as close-range cues for proboscis insertion by the long-tongued pollinators? That's David Attenborough's hypothesis essentially.
And we call that a proximate cue because that's about getting to the good stuff and solving the Rubik's cube of the flower, if you will.
But the ultimate reason why flowers would do this has to do with its reproduction. Does the presence of the markings somehow enhance the plant's reproductive fitness? Does that mean does it export more pollen so it sires more young as a male? And does it receive good high-quality pollen and produce fruits and seeds, which is its female function.
Remember that flowers, in most cases, are male and female. They're hermaphrodites. So that's another way that we have to kind of check our brains at the door about flowers. They're really different than us.
Begonias are more like us. They have males and females. But most flowers are hermaphrodites, and we can't relate to them.
So here's the experiment. This is a different kind of graph. This is a reflective spectrum. So these are wavelengths from the ultraviolet up to the red. And this is intensity and reflectance.
So when you look at the flower, the purple part here gives you this purple curve, a little bit in blue, a lot in the red, nothing in the ultraviolet. So this white on black arrow is the way we see it. There's nothing special in there that the flies see that we don't. That's what this is all about. And the black part really is black.
So here comes the high-tech manipulation-- Sharpie. (LAUGHING) This is a brilliant experiment. You don't need a grant to do this.
So there's the Sharpie, and what they did is they blacked out the arrows. So if you're going to do this experiment, and you're going to black out the arrows and then ask the flies to respond, there's something else that you have done by using the Sharpie. Sharpies stink.
So that was a sham control. A sham control is you take the Sharpie and you color the black parts over here. So everybody has ink from the Sharpie, and they all stink. And you wait a half hour, and the stink goes away. And then you do your experiment. And that's what these guys did.
So here's what happened. Do floral markings affect distance attraction, approaches, or close-range attraction? From a distance, there was no difference in the blacked-out ones versus the non blacked-out ones. And they measured distance by flies that came over the hill and then came zooming over to approach. That's what the data points are.
And then, close-range attraction really is about what proportion of those approaches ended in probing at the flower? There's a big difference here. When you take away the street sign, that doesn't happen anymore. That's pretty good evidence that close-range attraction is about having that high-contrast arrow.
Now, here the question is does the number of floral markings impact floral choice? Because in the previous one, you see, there weren't any white signs at all. They all got blacked out by the Sharpie. Here, what you've got is a kind of incremental increase-- none to one to three. And what this response variable is the proportion of choices made by the flies to flowers with the six full arrows.
So here, there is no contest. This one is a big negative. Here, when you've got one arrow, that's almost good enough, although there's still a 75%. Three out of four go to this. When it's got three out of six arrows, it's almost a coin flip.
And what they didn't do that I thought might be fun is if you change the symmetry and try to trip them up a little bit, but given how they responded here, I don't think that would really matter in the end. So that's the proximal stuff. The mechanism seems to work.
What about what it does for the flower? So here, they looked at export of pollen by using a surrogate. They took dayglow pink paint, another high-budget item, and dusted it on the surface of the flower.
And then they went out at night with a portable UV lamp and just counted how many flowers ended up with pink pollen on them. And here what they did was they cut off all the male parts, and they looked at does that flower produce a fruit three weeks from now? Did it get pollinated?
So here was what they found. When they blacked out the white arrows, only one out of those 20 flowers exported any powder at all. So not very good for the male end of things.
When they blacked out the arrows here, only one out of four, really, flowers produced any fruits, whereas this was more like half. So both for male and female function, those arrows really seem to matter. It's a pretty nice experimental demonstration of how things work.
So what happens when we add chemistry? That was a little sojourn away from chemistry for a bit, and now we're going to finish up with some chemistry.
Most flowers that are honest, most flowers that offer nectar or pollen, do it with combinations of odor and color.
And what I have here is a slide that kind of summarizes 25 or 30 years of work with honeybees in a way that kind of makes it simple to think about how honeybees can distinguish between different kinds of flowers.
So imagine a blue flower that had five odors. And the cell phone bar here are not really for that. Those are kind of the amount, relative amount, of each compound.
So this is a kind of five-odor blend that these blue flowers make. Imagine that a honeybee learns this blend in association with the color blue, and that's food for a week.
If you take the same color blue, the same five odors, and the same relative proportions to each other, but you ramp them up-- so you make them stronger or scented-- they can actually distinguish between the two of them. That's different to a honey bee. If you take the same color blue, take those same five compounds, and shuffle their relative abundance, that's different too. So that's a second way to be different.
So even living in a kind of conservative universe with only five scent compounds, we can come up with different ways to fool a bee. If you have the same flower, the blue color, the same five compounds in the same proportions and amounts, but you add a sixth compound, the yellow bar, that's new. That's something different.
And then, if you have the same five compounds but you change the color, that's a fourth way to be different.
So a lot of the work on honeybees has shown us that these can be easily learned and retained by bees for as long as those flowers remain profitable, as long as they offer nectar. Once they stop offering nectar, the bees can learn, oh, that's not a good place to go anymore. I'm going to mark that with my foot, and I'm not going to come back to it. And then they go finding something new.
Now, for the rest of what's left of my presentation, I want to talk about flowers that aren't honest. Let's start with flowers that lie to males. These are some of the most amazing orchids in the world. They're not large. And despite how beautiful these photos are, they're not showy because the flowers are no larger than a bee, a single bee.
So you can imagine what they're doing-- they are pretending to be female bees.
Now, depending on whose taxonomy you believe, there's anywhere from 25 to 100 species of these things around the Mediterranean Sea-- that's North Africa, the Middle East, and all of southern Europe. There's even some that get up into northern Europe.
And look at how different they are from each other. So you can just imagine what kind of pollinator space they're exploring. This is what we call a radiation-- not meaning cosmic rays or heat coming out of a device in your house, but when an ancestor of a plant or an animal gives rise to a starburst of different species as descendants.
Here's the idea-- that you have female bees and they produce a pheromone. It might be a single compound, or it might be the whole blend of odors that are on their skin, their cuticle.
Male bees don't do much. If you read about bees, male bees are not good for much. But they're very good at finding females, and they're very competitive once they do. Their time is brief, and they've got a job to do.
And so actually, these bioassays are very easy to do because you can take the essence of a female bee-- you can extract, for example, that word again-- and drip that extract onto a plastic bead. And that's good enough for the male. The male will fly to that bead, land on it, and try to mate with it.
And essentially, that's what the flowers are doing. So the flowers are kind of mimic, and the model that they're mimicking is a female bee. And it's obviously not just chemical because there's some really, really specific visual patterns on these flowers. This one in particular looks like a wing with a hairy body.
There's also orientation of the hairs. This is the labellum, or the lip, of the orchid. And the hairs on that are very important because they tell the bee where to land and where to put its front end and back end. And then this is the sexual part of the flower. It's going to put pollen packages onto the head of the bee.
In fact, do you want to see this? Yeah, let's watch this. Let's do that. Nobody's leaving the room. We can do that. Just give me a second to cue this up.
This is a very quick sojourn into the biology of figs, which we don't have to talk about. This just doesn't cue. But in a second-- here we go.
- Get a really sensational reward, a sexual one. They're little orchids, and their flowers reproduce remarkably closely the signals that enable a male bee or wasp to recognize a female of the same species.
Several have blue patches. One is fringed with what looks like fur. A wasp's wings in the right light do flash iridescent blue, and its abdomen is covered with thick, brown fur.
A female wasp also pumps out an identifying perfume, but the orchid does the same. And the result is irresistible. As the male wasp nuzzles forward in his attempts to mate, he butts the pollenia which stick to him like yellow horns.
He seems to be well aware that something has happened to him. But there's nothing he can do about it, and he flies off to try his luck elsewhere, which, of course, is what the orchid requires because this time, he deposits the pollen on another bogus female.
The hairs on many of these orchids run downwards as though the female is sitting with her head up. But some reproduce with her clinging head down. And then, the male must land that way if he wants to mate. And he will get the pollen stuck to his rear.
ROBERT RAGUSO: So you can see what I mean when I say that David Attenborough is an international treasure. These are incredible videos.
So let's look at how this works chemically. So here's the orchid you just saw-- Ophrys speculum. And here's the wasp that you just saw-- Campsoscolia ciliata.
And what you see here, the top squiggly line, is the chemistry of the female wasp. And the bottom squiggly line is the chemistry of the orchid. And what they have in common is this one compound. That's it. And that's the one.
None of this matters as far as he's concerned. And you can ask the wasp by recording from its antennae which odors does it smell. And then you can put that odor on a bead. And put it in the field when this plant is blooming, and they go bananas for it.
So in this case, it's a very simple case of a magic bullet, that the Ophrys speculum nailed the sex pheromone of that wasp. We don't know how. We don't know how. But it's got it right.
In this case, this is a different species. This is Ophrys sphegodes, and this is a different kind of pollinator. This is an Andrena bee. So it's not a Scoliidae wasp. It's a very different kind of animal.
And here, instead of having a single compound that's responsible for the sexual biology of the bees and the orchid, the orchid is covered with hydrocarbons, long-chain waxy hydrocarbons. They're barely scented. They don't smell like anything to you and me.
But what's happening here is that the lip of the orchid has basically reproduced the fingerprint pattern of hydrocarbons on the back of the bee. And the antennal traces down here show you that those compounds are the ones that matter. And so that's how this system works.
And what's very special about this is that once female Andrena bees are mated, they produce a kind of post-copulatory "leave me alone" odor. This is farnesyl hexanoate. You don't have to know this for the exam. But this is a post-coitus odor, and male bees stay away from that.
And what's fascinating about this system is that when Ophrys sphegodes is pollinated, it produces twice the amount of that compound. It's acting like a mated female bee. And that reduces the attractiveness of the flower. So there's half of the copulation attempts that you normally get when you add that odor to an otherwise popular flower. So that's a fine level of control on the system.
There's another one that's all about context. So here's another species of Ophrys-- Ophrys heldreichii. Here's what that looks like. Spectacular. And that's pollinated by a different kind of bee.
And what you see here is that when you give the bee a binary choice between two flowers, it prefers one over the other consistently. Maybe the ratios of hydrocarbons are more favorable in that one. For whatever reason, that flower is sexier than this one.
But when you take that sexy flower and you remove the purple petals around it, the perigone, that flower loses its allure even though the odors that attract the bees are not coming from those parts of the flower. And one of the interpretations of this-- it is a very simple experiment-- is that the Longhorn bees that are pollinating it, they look for females on purple flowers.
The time of year that they mate, the females of their species basically spend all their time on purple flowers. So that color is context for them. Maybe in their brains, it's triggering an enhancement of their response to the sex pheromone. So that's what we call context. And there's a lot of that in the pollination world.
One more video and then we're done.
- But the most punishing of fertilization techniques used by plants involve not sexual deception but imprisonment, penal servitude.
Gull colonies in the Mediterranean as anywhere else in the world, are busy, noisy places full of activity as parent birds come and go, tending their chicks.
They're also messy, smelly places with droppings, misplaced bits of half-digested fish and dead bodies lying about all over the place. In short, for flies and ants, they are very heaven.
And beside some gull colonies, you may find one of these. This is not an image of a sexy, seductive female animal. The mimicry is more gruesome. This is a bogus corpse, mimicking rotting flesh covered with hair and giving off the putrid smell of carrion. It's the dead horse arum.
Butterflies find this highly attractive. They need to find a hole to get into a corpse, and this seems to be one. Within are a whole cluster of tiny flowers. Those at the top are male but they're not yet ripe. Below is a barricade of spines. And below them, the female flowers.
Some of the flies have already visited such a flower as this and are carrying cargos of pollen. Down here, in a real corpse, they might have found succulent rotting flesh on which to feast and lay their eggs so that later their maggots could also feed, but they found nothing. As they continue to search, pollen brushes off of them onto the stigmas.
The spikes discourage them from getting out. By now, it's getting dark, and flies don't fly at night. They're stuck. During the night, the male flowers suddenly shed their pollen. And during the night too, the spikes of the barricade shrivel.
So by the morning, the flies are free to go. And each takes with it a load of pollen from the male flowers.
ROBERT RAGUSO: And off they go.
So let's take a quick look at how those flowers work, and then we'll wrap this up. Nobody's feeling like dessert now, are they?
So what attracts flies to these flowers initially is the small molecule dimethyl disulfide. There's very strong evidence now from many different studies that that's what flies smell, that's what the flowers make, and that's all you need to get them to come and land. Once they do land, however, you've got to get them into the chamber that you just saw. And they won't do that with odor alone.
What this set of experiment showed was that flies are more likely to enter the chamber if they walked down this rat tail appendix that you saw in the video. They're more likely to do that if it's hot. So mimicking a dead thing-- it's not good enough to smell bad. You've got to have the heat and the carbon dioxide and the hair, et cetera.
And what happens is when you make these things hot and add odor to them, you can increase the number of flies that walk down that staircase and enter the chamber. And that's what they need to do pollination.
Now, this carrion mimicry, this way of doing pollination, has evolved all over the world. So in southern Africa, there are wild milkweeds that do this. They don't look like milkweeds to us, but they sure are. In South America they are Aristolochias that do this. One of our Trilliums does this. Can you believe?
And in Southeast Asia, the two most spectacular flowers in the whole world, Rafflesia and the Titan Arum, are doing this. If any of you got to see the Titan arum in March, boy, that was a life experience for me. And all of our-- all 3,000 Ithicans who went to see it. This is an amazing, amazing experience.
So here it is-- the Titan arum. And we learned something really interesting about this flower that on the day that it opens, it waits till evening to really heat up. And what this is-- these are infrared photographs from 8 o'clock until midnight. And so the relative heat of the appendix part of the inflorescence here is indicated by color. The redder, the hotter.
So this thing is really heating up, and this is when it smells absolutely awful. But it surprised me because it's really evening and not during the middle of the day.
My students and I, when we were collecting some odor and temperature data as this flower bloomed in March, we read some of the few papers that were out there. And this paper from Germany basically suggested, based on biophysics, that what the flower is doing is it's like a chimney. It's using all of that heat and the shape of the inflorescence, which is like a big funnel, to create a convection plume. And it's sending that odor up into the forest canopy.
Whereas, if it were a low temperature, like a Rafflesia flower, and growing along the forest floor, what would happen at that time of day with the little movement of air that there is in the understory of a rainforest, is that the odor would basically blub along the boundary layer.
So what this suggested to me is that you can modify this signal, this little molecule that smells universally of dead meat, by putting it at different times, different places, adding heat, or not adding heat. And that might mean something different to different kinds of animals.
In fact, blow flies come to the Rafflesia but what comes to-- if you had more time, I'd show you the rest of the video-- what comes to these guys are stingless bees that are up in the canopy. So it's kind of splitting ecological niches by putting its odor in different places at different times.
And from South Africa, here's the best example of that. It's a little orchid. One more encore for the orchids. And this thing barely smells, but what it smells of is dimethyl disulfide.
And it's pollinated by a different group of blow flies-- not the blue, shiny ones that you get all over corpses but this little checkerboard sarcophaga fly.
And this graph simply shows that the dominant fly visitor of the three different kinds of flies-- houseflies, blowflies, and sarcophages-- the dominant visitor to the orchid are the sarcophages, these guys, checkerboards. The dominant visitors to carrion, like a dead possum, say, on the side of the road, are the blow flies.
But when you work with different sizes of carrion, these flies who make a living laying eggs in the carrion and competing with each other all the time, they've actually kind of split niches so that the sarcophages tend to use smaller dead animals than the blow flies do.
And so the niche of this orchid is small, dead animal. And it accomplishes that by having a small flower and a small amount of dimethyl disulfide. That's remarkable to me.
So let me draw some conclusions here, and if any of you still have any energy, we can do some questions and answers. The costs of lying if you're a flower, you get fewer pollinator visits. And so you may not be as fecund-- you may not produce as many fruits and seeds-- as an honest flower.
The risks of specialization for all flowers are that you're vulnerable to change. And the world is nothing but change. So you're vulnerable to climate change, your local extinction of your pollinators, or an invasive plant entering your environment and being more sexy to your pollinators suddenly, and something called negative frequency dependence.
What that basically means is if you cheat and lie, there can't be too many of you. You can't have a lot of Wall Street cheaters, insider traders because you crashed the system that you're exploiting. So one of the problems with being a parasite is you can't be too abundant because then you run out of hosts.
The benefits of deceptive pollination are that you might get a lot better outcrossing distances and get a lot less of inbreeding. And the reason for that is that at least for these orchids, male insects tend to move. Female bees and wasps that are tending a nest and foraging for honey, for nectar and pollen, they don't go very far. Hummingbirds defend territories, and they don't really move very far out of their territories when they're mating.
But male bees and wasps are vagabonds. So if they get one pollen package and fly a kilometer then do it again, that's the kind of outcrossing event you would never get with a female bee. So you might trade quality for quantity there.
Pollinator constancy via specialization. These guys aren't pollinators normally. So they're not going to go visiting daisies and lilies and other things. They're just going to come to your flower. So that's great because they're not going to waste your pollen on someone else.
And then finally, the idea of private signals. A nectar-rich flower that's purple and smells great might smell great to everyone, including animals that the flower doesn't want coming. And they might lose some of their investment to herbivory and to enemies. If you look like dead meat, you're not likely to get eaten by an antelope or a deer. That just stands to reason.
Finally, to draw everything that I've told you tonight to a close, we begin by asking, do plants behave? And I think that really begs the question of what is behavior? What I ask my students at the end of our semester is what do you think behavior is? The dictionary definition of behavior is something like this-- the actions or reactions of a person or animal or organism in response to external or internal stimuli. That's a pretty plastic definition. That could go for a lot of things.
I have shown you that plants communicate with themselves, with other plants, and to manipulate mutualists and enemies. They communicate with bacteria and fungi and with insects and birds and mammals. Plants anticipate environmental conditions in response to shade, heat, host odors, et cetera.
There's a lot of data from priming experiments that shows that plants that have experienced a previous event are much better prepared for the next event. So that's a kind of learning actually.
And so, yes, plants learn. They respond differently and reversibly to stimuli after they experience them. They just do it on a much longer time scales than we're used to thinking about and in ways that we don't do.
And so finally, not only do plants behave, a lot of organisms that don't have nervous systems or even multicellular bodies show those same kinds of responses. There's a lot of behavior in bacteria or in a slime molds, for example.
So really, in our courses, I use a lecture on plant behavior to get our students to think about behavior more broadly and to give active agency back to all the other organisms of the Earth that actually have it of their own accord, and we just don't normally think of them as being active participants in the game.
So I want to leave you where I started you, gazing across Cayuga Lake and thinking about, I hope, that plants are more than scenery and that when you drive past a forest or walk through it with your children or grandchildren or friends, think about all the conversations that are going on beneath your feet and over your head. Some of them have been going on for decades or centuries. And they're going to continue after you're gone. Thank you.
SPEAKER 1: That was an absolutely fascinating lecture. I feel like we've had a TED talk here. We did run a little bit late, but I think Professor Raguso could take a couple of questions.
ROBERT RAGUSO: Sure. Go ahead.
AUDIENCE: I heard [INAUDIBLE]
ROBERT RAGUSO: Can we have the mic for the--
ROBERT RAGUSO: There we go. Excellent.
AUDIENCE: Some people observe that in this beautiful picture here in Ithaca that not so many decades ago, that was all cut down. It's modern growth. And that there are rarer places now that we've been doing our thing which actually have hundreds of years or more of growth.
Do we know at this point if there's any difference between that communication underneath our feet in these young communities and those older communities?
ROBERT RAGUSO: Oh, that's a great question. You know, I try to remind myself that my grandparents, when they first got to the United States, were able to walk under chestnut trees-- I mean, dominant forests of chestnut. And they were Italian, and they loved chestnuts. So they thought, oh, great, we've come to a great country. We can have chestnuts all the time. And that was wiped out before my parents were even born.
We're going to lose ashes, I fear, before my children even know what one is. And so one of the big questions is about partnerships. Do mycorrhizae and other organisms in the rhizosphere-- are they flexible enough to choose different partners if there's a mass extinction or a pathogen that wipes out the partners that they have.
The flip side of that question is what kind of conditions make a benign organism become a horrific pathogen? I think that happens a lot. It's not my field directly. I know some of that literature to know that there's a bit of flexibility in terms of who the ecological players are.
I want to share a deep time or a shallow time anecdote with you about what we know about forests. How many of you have ever been to Bristlecone Pine Forest out west. OK, it's was a life-changing experience for me. This was the grove of the patriarchs in the White Mountains in California above Bishop.
And what I experienced was I walked up to this grove. And what you read about are the ones that are old and grizzled and have three needles left, right? They're just holding on to life.
But it's actually quite a vibrant and healthy forest. There's saplings. There's young trees. There is a conical Christmas tree, individuals a few hundred years old, et cetera. So demographically, it's a very healthy population. You have young to 4,000-year-old trees.
But what stunned me about being in that little grove was that there was fallen, dead wood on the ground that was as large and old as the ones that were alive. So if you could use dendrochronology and carbon dating, you could probably walk back, tree ring by tree ring, from 2012 to 12,000 years ago. That's stunning.
That mountaintop hasn't changed much. I mean, the glaciers have come up and down, but those trees have been there that entire time. And it's possible that some of the fungi that are living with them more or less have been there that entire time.
So I would put that as one endpoint on the continuum of a very old conversation. There are others that are going to be very fresh and young, as you suggest.
AUDIENCE: In the Stanford study that got publicized at organic [INAUDIBLE]
ROBERT RAGUSO: So the question is really about does organic farming change plant chemistry? That's such a new area. I mean, I could tell you about tomatoes. You know, the reason why we're willing to pay more money for heirloom tomatoes is they actually have flavor, right? So one of the really interesting consequences of plant breeding is similar to the consequences of animal breeding.
You know, what's the problem with German shepherds? Yeah, but they weren't bred for that. People didn't say, well, we're going to have hip problems, but let's do it anyway. Right? Tomatoes were bred in North America for color and shape and life off the vine so to have some degree of ethylene insensitivity, right, chemically.
But a lot of the chemistry I've been telling you about is metabolically or biochemically linked to other things. So when you breed a rose to have fewer spines or prickles or to last longer after you cut it, you breed out a lot of odor. So a lot of roses, now, presently, don't smell very good or don't smell at all.
Some of the most favorable, pleasant flavor compounds in tomatoes, ranked by human panels, are the ones that are related biochemically, structurally to lycopene, to the pigments that are the anti-oxidants that we value in tomatoes now that we know what they are.
So isn't that interesting that your sensory system as a human being tells you "like"-- you get a Facebook "like", right-- you like the odor that is the sawed head molecule of the anti-oxidant, that that gives you pleasure. That is such a profound question of what is pleasure from a biological standpoint.
We can end with that. How have you evolved as an organism to know what is good for you? And what does pleasure mean? I think that's where tomatoes bring us.
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Plants provide the life support systems for humans and all other animals on Earth, yet most people think of them as nothing more than scenery, or primarily as renewable commodities. However, biologists have begun to appreciate that plants play far more active, strategic roles in their own survival and success than was formerly appreciated, through adaptive responses to environmental stress and through complex above and below ground communication networks, mediated by chemistry.
As humans continue to explore the pharmacopoeia of secondary products produced by plants for their medicinal uses, biologists have learned that many of these compounds constitute an ancient language by which plants communicate with themselves, their neighbors, enemies and partners, on a time scale that few humans can appreciate. Professor Robert Raguso's talk explores these new discoveries and challenges the audience to listen to their gardens, forests and meadows with new ears (and noses).