The femme fatale Photuris. Photo by Bruce Marlin; click image for Creative Commons license and image source.

If I read my notes correctly, Thomas Eisner once had a pet thrush named Sybil who rejected only five insects out of the hundreds the entomologist offered her. They were all beetles. And one of them was a firefly.

For any other bird owner, this observation would have simply limited their pet’s meal options. But this was Thomas Eisner — one of the great entomologists and chemical ecologists of the 20th century. To him, it was a tantalizing clue, and he decided to find out what made the fireflies have all the thrush plate-appeal of haggis. What he stumbled onto was one of the great new natural history stories of the 20th century — and the latest in a string of Eisner’s greatest hits.

I know this because in fall of 1998 I was a student in BioNB 221 — Introduction to Animal Behavior — at Cornell University. Eisner, a professor at Cornell, taught the last six or so lectures, which I still have preserved in my notes. What I did not know at the time, and did not learn until afterward, was that Eisner was one of the great biologists of the 20th century. I found this out in later years, when his discoveries were featured in many an article at the New York Times, where I had a mysterious feeling of deja vu.

What I did know at the time was that I could not take my eyes off the screen while he was lecturing. I’m a fan of a good natural history story, which you may perhaps have gathered. Eisner — who was once E. O. Wilson‘s college roommate — was overflowing with them — and in many cases, because he’d figured them out himself. Sadly, Eisner died March 25. You can read more about his life in this fine remembrance by NYT reporter Natalie Angier*, whose daughter was lucky enough to inherit the contents of Eisner’s old burlap field bag and was, frighteningly to me, born around the time I sat listening to Eisner’s lectures. Angier wrote about his life. I want to share with you a few of the natural wonders I learned from him, sitting rapt in the darkened Uris Hall auditorium.

This Means War

Eisner’s specialty was the world of chemical warfare among plants and insects. Insects produce, steal, and reuse chemicals from plants and each other constantly. Millipedes can deploy hydrogen cyanide, whip scorpions acetic acid, and ants formic acid, but for Eisner, the poster child for entomological chemical defense was the bombardier beetle. “If you live on the ground,” he said, “you must either take flight quickly or defend yourself instantly.” The bombardier beetle went with option B.

The beetle takes chemicals called hydroquinones, mixes them with hydrogen peroxide and catalytic enzymes (peroxidase and catalase) in a reaction chamber in its hinder, and uses the resulting explosive formation of benzoquinones and heat to persuade frogs, ants, and spiders that their best meal options lie elsewhere.

Using grainy films he had shot himself, he showed us how beetles touched with probes could deploy a vicious defense with pinpoint accuracy in nearly any direction. He suspended the beetles over pH paper, so the 100°C benzoquinones they released would reveal their precision firepower.

This British film (which seems to have been created by intelligent design advocates who tried to abuse Eisner’s research for their ends**, so ignore the bit at the end. I couldn’t find another version, unfortunately.) incorporates some of the movies I saw that day, as well as explains how the beetle uses physical barriers to control its chemical defense system. I think you can even see Eisner in one of them for a few seconds at the end — he’s in the foreground.

And here’s David Attenborough describing the beetle in HD:

Don’t Feed on Me

Plants, too, load up on poison in hopes of warding off the hungry crowd. Nettle spines are filled with irritating chemicals, as are the latex canals or resin canals of flowering plants and conifers, respectively. Some plants store poisonous chemicals in their tissues like caffeine or nicotine, which in spite of their uplifting effects on humans, are actually insecticides.

But some insects have picked up on this gig, and begun using it to their advantage. Sawflies slice into the resin canals of pines and steal the sticky sap, storing it in special sacs for defense against ants. Monarch butterflies sequester milkweed toxins from their food, rendering themselves distasteful to predators. Assassin bugs coat their eggs with the noxious excretions from camphor weeds. Their young then reuse the chemicals for defense and to catch prey. We do this too, Eisner pointed out, by stealing the defense chemicals from fungi and other bacteria. We call them antibiotics.

Eisner told us of plant chemicals stolen and presented as nuptial gifts among moths, where female choose males whose flirting, aromatic antennae tell them they have stored the most alkaloid derivatives. That implies the male is both fittest and has the most to give to the pair’s offspring. For if the female mates, the male will transfer not only his sperm, but his alkaloid collection, which the female will carefully store with her eggs for the use of her young. Other moths do the same with salts they siphon from puddles.

And he told us of the evesdropping of kairomones — chemicals that, unlike pheromoes, used for intraspecies communication (like the moths), or allomones, which benefit the emitter of an interspecies pair (like the benzoquinones of the bombardiers or the stinking of skunks), benefit the receiver and betray the emitter. Think, for example, of the carbon dioxide that gives you away to mosquitoes; any scent, really, that betrays prey to predators can qualify. Eisner called it a “chemical gestalt”, the effect of “inevitable chemical leakage”. But the tables can also be turned. Predatory rotifers called Asplanchna unwittingly emit chemicals that alert prey rotifers called Brachionus to grow defensive spikes (read more about rotifers from this blog here and here).

One of my favorite Eisner stories, one that has especially stuck with me all these years, was about true bugs entomologists were attempting to rear in petri dishes on damp paper towels. The bugs’ development was, however, stalling; they could not be coaxed to adulthood. The scientists were baffled. Until, that is, someone noticed the paper towels were made from balsam fir, a tree that emits allomones to stunt insect development. This chemical was, apparently, surviving the paper-making process and continuing to thwart the trees’ insect enemies — even in death.

Bolas spiders use imitation pheromones — another allomone — to lure male moths in search of a date (the females, apparently, are immune to the spider’s charms). This video depicts the unfortunate result:

You may have heard of parasitoid wasps — the Alien-style predators of spiders, caterpillars and other insects that lay their eggs in their prey, where the young maggots proceed to devour their hosts’ organs while still alive before finally using their hosts’ spent husks as pupae from which young wasps emerge. But perhaps you did not know that some plants injured by caterpillars or aphids call out chemically to parasitoids to defend them. But the story gets better; the immune system of the host in some cases is destroyed by viruses injected by the parasoitoid wasps along with their eggs. “And(I underlined this in my notes) the viruses have also been incorporated into the wasp genome.” To which I further wrote, “1 organism now? Whoa.”

He told us how mammals, too, use pheromones. Babies can distinguish their mother’s milk from others, he said, and the scent of male armpits can regularize erratic female ovulation. In mice, the scent of strange male urine blocks implantation of fertilized eggs in female mice; the effect and reason may be similar to an article I just saw last week about mares aborting fetuses to save themselves investing energy in foals likely to be killed by rival stallions anyway. This could explain the spectacularly high miscarriage rate in mares (around 30%) who are trucked out to mate with top stallions but housed while pregnant with other males. That this is likely to have not one whit of effect on the way breeders practice horse husbandry is testament to the often hidebound thinking of humans.

The Bee-Letters of Flowers

But on top of all this research into chemical crossfire, Eisner also dabbled in the world of light and visual communication. Those who have studied physics know the electromagnetic spectrum of which light is a part is a vast array of energy. Earth’s atmosphere filters much that arrives, and most of what makes it through falls in the 320 to 2300 nm range. What we perceive as visible light falls in the 380 to 750 nm range. But that leaves a large part of the spectrum invisible to us. What if other animals could see different colors or different parts of the electromagnetic spectrum? As it turns out, they do.

We cannot see ultraviolet. But, through experiments worked out by a whole host of Germans, we know bees do. Conversely, bees cannot see red. Their vision lies in the 340 – 650 nm range. Blue, red, and green are the human primary colors. But the bee primary colors are yellow, blue, and ultraviolet. That implies there are a spectrum of colors that they see that we cannot. My mind bent a bit as I heard this — there’s a whole world of color out there that we can’t see!

And those colors needed names. Yellow + blue we can see along with bees — we call that blue green. But what about blue + ultraviolet? That was dubbed “bee blue”. Yellow + ultraviolet? “bee purple”. And, as it turns out, flowers are adorned in these shades, invisible to us but brilliantly displayed for bees. Flowers probably first used UV-absorbing pigments as sunscreen, Eisner said, and only later turned to them to decorate their petals. Now, bee blue and bee purple form pollen guides for bees, often flecking the tips of flowers and leaving a yellow disc in the center as a bullseye. You can see the effect in this photo collage of black-eyed susans with ultraviolet tips and a yellow center, though the bee would see both yellow and ultraviolet simultaneously as bee purple.

Cucumber flowers in natural light(left), and in ultraviolet falsely colored yellow(right). To bees, the flowers would appear bee purple with a yellow target -- the pollen guide. Creative Commons kevincollins123. Click for license and link.

The inability of bees to see red means that pink are red flowers are almost never pollinated by bees. On the contrary, only butterflies and hummingbirds — which are not red-blind — are attracted to red flowers. Eisner wrote papers about his experiments in this world as well, examples of which you can see here and here.

Which brings us back to what is likely his most famous experiments in light communication — the Tale of Photinus and Photuris. Following up on the expectorated clues provided by Sybil, Eisner extracted chemicals from the fireflies with various solvents. He discovered that the firefly she spat out — Photinus — contained a steroid called lucibufagin. When fireflies are caught, they “bleed” hemolymph full of this chemical. Spiders who catch and taste them let them go. They even release fruit flies merely painted with the chemical, the scientists discovered. Eisner found Photinus was chock-full of the chemical right from the start of the season. A larger firefly, Photuris, also contained this chemical. But only the females. And only later in the season. He began to glimpse the truth of a dark story.

Male fireflies searching for females make a species-specific pattern of flashes. Females respond with a single blink, but with a species-specific time delay from the male call. Photuris, coveting the chemicals of Photinus, imitates that response. When the male lands thinking he is about to get lucky, he gets eaten instead, and the female accumulates the chemical that allows her to escape predation by spiders and yes, thrushes.

How could one man do and learn so much? Perhaps because he never let the Lab get in the way of Life. This passage from Angier’s piece, in particular, explains why I love Eisner — and to a large degree why being a modern biologist was not for me.

Ian Baldwin, a professor of molecular ecology at the Max Planck Institute for Chemical Ecology in Germany, who studied with Dr. Eisner  in the 1980s, said of his mentor: “He articulated the value of natural history discovery in a time of natural history myopia. We train biologists today who can’t identify more than four species, who only know how to do digital biology, but the world of analog biology is the world we live in. Tom was a visionary for nonmodel systems. He created narratives around everything he did.”

In today’s “shiny polished science world, he was proof that there is no experience that can substitute for being out in nature,” said Dr. Berenbaum. “It’s classy, not low-rent, to stay grounded in biological reality.”

Thank you for the stories, Dr. Eisner, wherever you are.

____________________________________________________________
*My answer to the question of “Who are your favorite science writers?” with “Natalie Angier” probably terminated my interview for a science journalism internship at a major daily newspaper about seven years ago. The editor seemed to lose interest in me at that point. I wasn’t going to lie, and I’m still offended on her behalf.

** Indeed, they have also done so to my graptolites post. They linked to my blog post as part of a post using graptolites as proof of “stasis”.

But before we take a closer look, let’s take a step back . . .

Hallucigenia at the Smithsonian, Washington, DC. Creative Commons jylcat.

This is Hallucigenia. It is an odd creature, one who has been reconstructed both right side up and upside down (presuming only one of the directions was correct in real life, which given the general weirdness of early life, may not be a safe assumption), and which of the two the current reconstructions is correct may still be anyone’s guess. It has been interpreted variously as walking on pointy tentacles with flexible feeding arms on its back, or walking on flexible feet with pointy spines on its back (the currently favored interpretation, pictured above).

It was such an odd duck that the famous paleontologist Simon Conway Morris, whose study of bizarre Cambrian animals in the Burgess Shale Stephen Jay Gould wrote about in the book Wonderful Life,  named it after a hallucination. Morris also happened to originally reconstruct the animal in the currently non-accepted fashion, meaning perhaps that with creatures so strange, even great paleontologists can be fooled (we saw that that was the case for Anomalocaris too).

Hallucigenia was probably a lobopod, a type of creature with hollow, lobe-like legs that are extensions of the body wall. The fossil beds are full of strange incarnations of lobopods, some of which you should see here, here, and here to get a sense of the variation and general weirdness in the group.

But the creature debuted this week in nature may take the cake. (Alas — I lack copyright permission to use the images, so check out Ed Yong’s photos of the fossils here.) One cannot help but compare Diania to a first-grader’s pipe-cleaner art project. It is shockingly, wonderfully, delightfully weird. Can you imagine this thing shambling along the bottom of the Cambrian* oceans? What was it eating? How did it . . . er. . . make little walking cacti?

Aside from the delight that their sheer beauty and knowledge of their existence inspires, these organisms are important for another reason. They may have been among the ancestors of the arthropods, the tremendously successful joint-legged creatures that include insects, millipeds, and crustaceans.For, true to name, they appear to have hardened, jointed legs. But unlike arthropods, their bodies are not. The authors of the paper in Nature that revealed this creature to the world suggest that that may mean jointed legs came before jointed bodies, meaning the name “arthropod” (jointed foot) for the group was well chosen indeed.

Scientists were especially excited by the find because they had lacked any intermediate forms between the apparently soft-bodied lobopod fossils and the stiff and jointy arthropods. This looks like evidence of life in that transition.

What would Diania have looked like in real life, and how would those spindly legs have moved? Living lobopods — the modern day relatives of Diania — might give us a clue. Today, there are probably only two surviving members of the lobopod group — the velvet worms,

Creative Commons teague_o. Click for link and license.

and the water bears, or tardigrades (remember?). Tardigrades are the foil-hatted survivalists of the animal world, withstanding pure alcohol, the vacuum of space, temperatures from -272 to 149 degrees C and ionizing radiation with remarkable aplomb. It’ll be them, cockroaches, and twinkies in the fallout of the apocalypse. Yet belying that ability is their adorable plush appearance, as they trundle along on their cute little claw-footed stumpy legs, as you can see in this video.

They can live practically anywhere — from moss to the deep sea to hot springs.

Velvet worms, on the other hand, are skilled predators with an incredible way to snare their prey. As usual, David Attenborough puts it best in this video:

This is a little animal called a water bear, or tardigrade. On the mosses, lichens, forest litter, ponds, beaches, snowbanks (and even hot springs) of the world, this little guy plods along, oblivious to the larger world. At just 100 micrometers (.1 mm) to 1.5 mm long, they are cute on paws. Did you notice the little fingers?

Hug me! The caterpillar from Alice in Wonderland meets Heimlich from A Bug's Life? Creative Commons Rpgch

Discovered in the 18th century, these little guys were named water bears for their trundling, bear-like gait — that is, if can you imagine a bear with *four* pairs of legs and a penchant for shriveling up in winter rather than curling up in a cave. Tardigrade, in fact, just means “slow walker”.

Water bears exist at a strange junction between the world of the large and the world of the small. They are multicellular organisms with intestines, brains, eyes, fingers, and a chitinous cuticle that they shed, but in many ways they behave like protists, which are also microorganisms but not animals at all. Some tardigrades don’t defecate until they moult. Others don’t mate until that happens. The fertilized eggs stay behind in the moulted skin and incubate there, or sometimes adhere to a nearby surface. They are also eutelic (you-tell-ik), which just means that every water bear grows exactly the same number of cells, and once that number is reached, they can grow larger only by growing those cells. This isn’t uncommon for microbial life. Their mouths are armed with stylets with which they pierce and suck the delicious contents of plant cells, algae, and small invertebrates.

Creative Commons Rpgch

As for their bizarre survivalism streak, withstanding the vacuum and scorching solar radiation of space seems to be a byproduct of their ability to survive dry spells (they can go for a decade without water), just as it is for the bdelloid rotifers, whom I’ve also covered here. They can reversibly enter a state of suspended animation called cryptobiosis, in which their metabolism screeches to a halt and their water content plunges to a hundredth of normal. This helps protect their DNA, and a sugar called trehalose helps protect their membranes. For further information, see here. In 1997, they were launched into low-earth orbit and survived the vacuum of space for 10 days. Yes, Tardigrades . . . in . . . Space! Several went on to lay and hatch eggs normally. Interestingly, there is even a sci-fi sounding word for their state of suspended animation: when so ensconced, they are called a “tun”.

Taxonomically, water bears are most closely related to arthropods, or all the crustaceans and insects of the world, and onychophorans, the velvet worms. Biologists would say they are one of the bilaterian crown groups, or one of the earliest lineages to split into their own group after animals developed mirror-image symmetry. Other early-diverging animals either had no symmetry (sponges) or were radially symmetrical (jellyfish et al.) You can check out their neighborhood of the life family tree here (look for tardigrada). You may notice they’re also in a group called “ecdysozoa”, which is just a code word for “all the organisms that moult exoskeletons”, which actually does seem to be a true, historical, one-time evolutionary inovation (i.e., synapomorphy in bio-speak), and thus make it a taxonomically valid group.

Final cool factoid: few tardigrades have fossilized, but of those that have, one was named Beorn leggi, which will be delightful to those of you who have read The Hobbit. And in case you were wondering if someone actually had the chutzpah to do it, yes, yes someone did. It was screaming to be done. Behold the plush tardigrade.