Manipulative Bounty

It is late summer in western Oregon, meaning the wild blackberries are just ripening, dangling tantalizingly between the wicked thorns of canes that can arch up over fifteen feet in the air.  The canes form thickets impenetrable to animals larger than rabbits.  Come and get it- just don't forget your machete and a willingness to make a small blood sacrifice.

We don't give plants much credit for intelligence, at least not as we typically define it, but the dark, sweet fruit is all about making up for the one thing plants sorely lack once they've put down their roots: mobility on a time scale relevant to getting your kids out from underfoot.  Trouble is, if you dump your offspring right around your knees, you're liable to kill them by outcompeting them, for space, water, and especially light. You are also a magnet for seed predators, waiting for the bounty to fall.  So, somehow, plants have to get their seeds away from them.

Some plants have gone the engineering route, and over time natural selection has outfitted them with pods that burst open, giving their seeds the equivalent of a blast from a cannon, or lightweight parachutes to help them drift away.  These plants don't ask for help from another living organism.  Some plants produce seeds that float to new locations, like coconuts.  Other plants have done some modified engineering, covering their seeds with sticky coatings or grapple hooks to catch a ride on any passing animal.  They are the freeloaders, getting a lift on the sly and offering no compensation for the service.

Jewelweed, Impatiens capsensis, has exploding pods, earning it a second name, touch-me-not.  Photo by Catherine Khalar

But plants with fruits definitely do ask for help from organisms that are capable of quick movement.  They pay a fee up front, and hope the agent delivers the goods as planned.  In short, fruits are a biological bribe.

The intended agents are those animals whose guts digest the fruit but leave the seeds unharmed.  The time it takes to process the meal helps guarantee a final deposit away from the parent plant, protecting the seeds both from infanticide and from the usual buildup of seed-eating insects or fungi that prey on the fruit that drops to the ground from the parent plant.  Think of an untended feral apple tree.

Some plants have evolved to rely primarily on birds to disperse their seeds.  Bird fruits are typically fairly small so they can be swallowed whole, and are often black, blue, or red and placed out on the ends of slender branches.  Other fruits appeal more to mammals, with big green or pale yellow fruits, often with an odor.  Many other plants outfit their seeds with small fleshy bodies called eliasomes, that appeal to ants.  The ants take both the seed and the eliasome back to their nests, where the elaisomes are consumed and the seeds are discarded, often in a safe underground spot perfect for germination.  Even fish eat fruit.

The fruits of salal, Gautheria shallon.  Photo by J. A. Gervais

Some fruits are simply weird, such as the osage orange.  If you've never seen one, it is a fruit the size of a softball and about as appetizing.  You need a hammer to crack one open.  The Missouri Department of Conservation considers the fruits hazardous and advises wearing hard hats in their vicinity.  In her engaging book The Ghosts of Evolution, author Connie Barlow makes a compelling case that such fruits actually are anachronisms, whose main seed dispersers were now-extinct large mammals and possibly even dinosaurs.  These fruits now "disperse" by crashing to the ground and possibly rolling away a little, sometimes helped along by flowing water.  Seed dispersal isn't an exact match of goods for services.

There are plenty of cheats, too, animals or other organisms that take the payment without delivering the goods.  My goats eat blackberries with gusto, but no seed will survive the ghastly conditions of their rumens.  Fungi readily infest fruit, and usually also destroy the seeds.  I've found that banana slugs eat fruit, but they damage a percentage of the seeds they eat, taking a higher payment than planned for their services.  The plant has to offer enough fruit to ensure that some of it falls into the right mouths- the first step, but only the first step, in the chain of events that will ultimately lead to a new plant that will someday produce its own seed.

Animal delivery may also come with a secondary benefit.  Tapirs in South America use latrines, small areas of communal relief.  Along with the rest of the waste, they deposit the seeds of the palm, Maximiliana maripa. Over time, these turn into stands of fruit-producing trees.  Tapir poop, too, seems to discourage the beetles that eat the seeds.  Ant garbage dumps are excellent germination sites for many plants.  Bear poop contains thousands of seeds which later germinate in the clumps of calling cards the bears leave behind.

Black bear fattening up on blueberries, Sol Duc wilderness, Olympic National Park. Photo: J. A. Gervais

Hot peppers are my favorite example of botanical craftiness.  Hot peppers get their kick from a compounds called capsaicinoids, which includes capsaicin.  The capsaicin triggers a specific receptor in mammals that is infamous for its response.  It is used in many different cuisines around the world, and also mace (something to think about when contemplating how spicy-hot you want your meal).  Turns out that peppers use birds as seed dispersers.  Birds can't taste capsaicinoids because they don't have the receptors- no tear-gas effect for them.  The compounds do, however, affect how quickly the birds' guts process the meal, shaping the rain of seeds over the landscape, and preventing a huge pile of seeds  from being deposited all in one place.  When that happens, most of them die from the competition.  The capsaicinoids also protect the fruit from attack by fungi, which would destroy the seeds.

The blackberries that are so common locally involve another twist.  They are an exotic species, Rubus armeniacus, originally from the Himalayas.  In open areas with plenty of sun, they can overgrow small buildings, abandoned cars, and nearly any other plant.  They also produce prodigious quantities of very tasty fruit, which feed nearly every wildlife species in the area judging by the bright purple bird droppings deposited on the car and mammal scat along trails in the woods.  Those seeds really get around.  The plant is a pernicious challenge to people trying to restore meadows, pastures, or stream forests. 

The blackberry thickets provide shelter and food to small mammals, birds, and reptiles in the forgotten wastelands that have been badly disturbed, but never rehabilitated or fully claimed by people.  At least the thickets are a good fortress against free-roaming cats, and offer a terrific late-summer energy boost to birds about to migrate.  They also provide us with an abundant supply of local fruit for the freezer, and blackberry jam in midwinter is one of the finest wild gifts we receive from the woods and fields around us.

Blackberry thicket overgrowing a roadside.  Local bunnies taunt the dogs from under this natural razor wire. 

Photo: J. A. Gervais

Bananas in the woods

It is finally getting warm here in western Oregon, but it is still very humid so the banana slugs (Ariolimax columbianus) are still active.  I have a soft spot for banana slugs.  The idea of a six-inch long monster yellow slug that looked like a piece of overripe fruit seemed too far-fetched to believe when I knew them only by reputation.  I was delighted to find them just as large and spectacular in life as legend made them out to be.  My interest in them from a biological point of view began while I was doing research for my Master’s degree, on the seed dispersal dynamics of salmonberry in the Oregon Coast Range.  One rainy afternoon in early June, I looked down and realized there were a dozen massive slugs slowly working their way through the tangled vegetation within the bounds of my one-meter-square quadrat.

Photo: National Park Service

That’s a lot of animal when you look at it from a biomass standpoint, even if the animal possesses a very slow metabolism.  Slugs eat everything, from fungus and fruit to their dead kin and other animals’ feces.  Mostly they are herbivores.  Work in the 1970s demonstrated that slugs can affect plant community composition in the forest understory.  They also act as a host to a number of generalist parasites (another good reason not to eat one, even if the slime didn’t put you off), and they likely disperse the spores of fungi as well.  In other words, slugs do stuff to their environment. 

I found salmonberry seeds in their droppings and asked the obvious question: are they seed dispersers, or seed predators?  I set up ten Tupperware slug houses, raided the nearby forest for volunteers for science, and kept ten slugs going on potato, carrot, and fresh lettuce in addition to the salmonberries and other wild fruits in my living room.  You could actually hear the slugs chewing.  Fortunately, my roommate thought this was intriguing if a bit weird.  After the animals obligingly ate a series of fruits from the local forest, I let them go, perhaps a bit fatter than they were before.

Salmonberry (Rubus spectabilis) and its two color morphs. Photo: J.A. Gervais

I planted the seeds, and discovered that banana slugs do disperse viable seeds, although their gut kills some of them.  Interestingly, red salmonberry seeds were more likely to die during gut passage than orange ones.  All of the other seeds from native plants producing fleshy fruits also were capable of germination.  I tried to use the word “molluschrory” to indicate this novel dispersal agent of seeds, but my co-author on the paper, ecologist Mary Willson, shot that down.  It is hard to have your tongue in your cheek in a scientific paper, apparently, and have others get the joke.

Slugs aren’t the most spectacular seed dispersers, because in the twenty four hours that it takes them to pass a seed, they don’t go very far.  In fact, slugs have fairly small home ranges with a number of shelters that they will return to repeatedly, following their own slime trails around their neighborhood.  The slime they secrete under the muscular foot is astonishing in itself.  Slugs change the chemistry of the slime according to their needs, secreting a more watery version when traveling along the ground, a tough cord they use to rappel down from the heights of a shrub, and thick viscous goo to deter predators.  They can change the composition of the slime to fit the circumstances, and the chemistry can be altered in a matter of minutes.

Predators can track the slugs from their trail of slime, so their trails may work against them.  One slug, the jumping slug (several species in the genus Hemphillia) actually twists off its slime trail, breaking the chain of evidence a predator might use to track it down.  Another slug, the tail-dropper of the genus Prophysaon, drops a bit of its tail to distract a predator while it makes its getaway.  I am not making this up.  The banana slug has no such defense, and must either outrun or hide from its enemies, which include predatory ground beetles, snakes, Pacific giant salamanders, and even other slugs.  You can blink more than once while watching a predatory slug hot on the trail of a fleeing banana, but it is still a race of life and death for the participants.

The magnificent blue-gray tail-dropper (Prophysaon coerleum), photo: USDA Forest Service

Scientific literature is not often very amusing, but one of the best papers in my collection describes how to individually mark slugs by freeze branding them.  The publication included illustrations of miniature brands and instructions on how to use dry ice to do the deed.  The spotted slugs’ markings are unique to the individual, so photographic records work for identifying them.

Getting to know slugs as individuals revealed that banana slugs can reach at least six years of age in the wild.  They aren’t prolific egg layers, relying on their longevity to produce enough young to carry the species.  Simply put, a nice-sized banana slug may be older than the vast majority of mammals on earth.

 The study of banana slugs pretty much petered out 30 years ago, although the Northwest Forest Plan did at least pay them lip service in terms of requiring that forest managers survey for them.  It is good to remember there is a great deal we don’t know about our fellow travelers, even the ones right underfoot.  Step carefully.

Trillium

Trillium chloropetalum, the sessile trillium or wake-robin, flowers in mid-March in the woods of western Oregon.  It blooms just before the start of the spring chorus of birdsong.  This plant's mottled leaves are  almost as showy as its greenish-white flowers, which don't open into broad showy blooms like the western trillium. Both species of trillium produce a seed with an eliasome, a fleshy body particularly attractive to ants who disperse the majority of the seeds.  Yellow jackets also disperse trillium seeds.  These plants are pollinated by beetles, bumble bees, moths, and the non-native honeybees.

I didn't find any published research on the sessile trillium, but the western trillium can live to be over seventy years old based on counts of the annual restrictions on its rhizome. It does not even begin to flower until its fifteenth year. Trilliums don't survive disturbances such as logging, and the increased numbers of mice associated with clearcut and edge habitat take a toll on their seeds.  Long-lived, slow-growing plants affected by human disturbance face an uncertain future.

Even so, the sessile trillium persists in some unlikely places.  Along the overlooked urban banks of a local river, a thin strip of trees between the pedestrian path and the water's edge ducks under a series of overpasses.  Scotch broom, English ivy, and Himalaya blackberry tangle old plastic bags, broken bottles, and other refuse in the understory.  Nobody looks to these places for conservation.  But sessile trilliums bloom here every spring, refusing to relinquish this patch of forsaken ground.

Trillium chloropetalum. Photo by Linda Hardie-Scott

They remind me of the hand-held candles used in protests and memorial services, the flame borne above a flimsy shield.  These past few weeks have been marked in the human world by much upheaval and anguish in many countries torn by civil war, government violence against the unarmed, and the disasters in Japan.  The Japanese ceremony of floating candle lanterns, Toro Nagashi, honors the dead.  The trilliums blooming in the local woods have their own purpose, but they are still bright spots of both hope and memory in these dark times.