Botanical Ballistics: There’s a War Going on Out There

By Kristen Nelson

In many areas of coastal California, the rolling hills are awash with green for what feels like the first time in years. It’s as though the much-anticipated fall rains were accompanied by drips from an artist’s paintbrush, splashing down and spreading out in rapidly-expanding, pigment-laden circles as they absorbed into the parched earth. For any outdoor enthusiast, the rain and accompanying burst of life and color were welcomed enthusiastically. The greening landscape foreshadows the long, warm days of spring filled with wildflowers and wanderlust. It’s not all fun and games (and blowing off school work for beach volleyball) though. For some, it’s time for war…

Rally the troops, it's GO time!

Allow me to explain. As the days get longer and warmer, plants of every shape and size (or at least all of the spring-blooming species… which is most of them) are signaled to prepare for reproduction. This means cutthroat competition for resources, space, and pollinator attention, followed by a frenzied race to disseminate the next generation of seed. For annual plants, the pressure to successfully reproduce is particularly great, as they only have one shot to get it right. In other words, it’s GO time. Now, I know what you are thinking… PLANT warfare?! That sounds about as menacing as a slap fight...

  

But let us not forget that plants must acquire food and water, have sex, make babies, and spread their seed from a stationary position! The diversity of mechanisms evolved to make all this happen is flat-out mind-blowing. You don’t have to take my word for it though. Allow me to introduce you to one particularly badass little herb that goes by the name filaree (Erodium spp.).

Oh hey there little guy... what's your name? 

Kinda dainty and pretty cute… right? WRONG! This conniving little warlord rains tyranny down on grasslands (as well as many other habitats) throughout the world every spring. How, you might ask, does our little friend filaree accomplish this? Explosions, botanical ballistics, and hygroscopic coiling. That’s how.

Deceptively harmless, secretly menacing.

Here’s how it works… each filaree flower produces a fruit that consists of five seeds, each attached to a long awn. (An awn is a slender, bristle-like appendage that typically functions in seed dispersal.) The five awns of an immature filaree fruit are fused into a column (See photo below, left). As the fruit matures, the awns dry out and separate from each other along longitudinal perforations. Check out the photos below to visualize the structure of a filaree fruit.

Six immature fruits, each with column of fused awns.

Mature, dry fruit, with one awn coiling and breaking free.

Filaree awns respond to small changes in local humidity by coiling and un-coiling which allows it to explosively disperse up to a meter from the parent plant, crawl along the ground in search of a suitable crevice to crawl into, and then screw itself into the soil, where it lays in wait for the next rains. Did you catch all that??? The filaree plants itself in the soil! I can tell you’re not impressed, so let me show you…

Self-burying Erodium Seed  (ßyou have to click the link… it’s worth it… do it! Action begins at 12 sec.)

The internal structure of the awn is what allows the filaree to accomplish these tasks with such impressive elegance. The long, narrow cells of each awn are arranged parallel to the length of the awn (see image below, left) and each cell has a microfibril (I will just call it a fiber) made of cellulose that wraps around it in a helical pattern. Now, in a normal/generic plant tissue, these fibers coil around cells such that the axis of each coil is perpendicular to the axis of the cell (picture a slinky with an oblong cell placed in the middle of it). In the filaree awn however, fibers coil around the cells along a tilted axis. Check out the diagram below (right) to help visualize the difference….

Longitudinal section of awn.

(a) Normal microfibril arrangement perpendicular to cell axis (shown in red);
(b) tilted axis of microfibrils (shown in yellow) as in a filaree awn.

The tilted axis model is key because it creates an angle between the cell axis and the fiber axis that allows for coiling of the entire awn. Picture each cell of the awn as one of those long skinny balloons that circus clowns use to make balloon animals. When an awn is wet, water fills all the free space between cells and within cell walls, causing each cell to swell like a full water balloon. This causes the awn to straighten (just like the balloon would). Now, poke a tiny pinhole in your balloon so water drains out really slowly. As the awn dries out, the cell wall shrinks – but the fiber attached to it maintains its size and shape, causing the semi-deflated cell (balloon) to twist at angles perpendicular to the fiber axis. When many adjacent cells all do this at the same time along a tilted axis, it causes the entire awn to coil up into a helix. Here is what it looks like when an awn goes from wet to dry...

This video is a timelapse of ten minutes:

Now it’s time talk explosions. When an awn is dry, it wants to be in a coiled state (that is the energetically favorable shape). However, when the five awns of an intact fruit are fused into a column, they are forced to be straight. As the fruit dries, tension builds up in the five connected awns because their cells are losing water and beginning to twist. Eventually, enough tension accumulates to separate the awns, resulting in an explosive release of energy that catapults the awn up to a meter away!

Watch closely...

Don't even blink for this one...

Once dispersed on the ground, daily changes in humidity cause the awn to repeatedly coil and uncoil, allowing it to crawl along the ground in search of a crevice or hole (as in the first video). Stiff bristly hairs on the seed and awn help pull the seed along. And in the event that successful planting doesn’t occur, the bristly hairs aid in fulfilling plan B – catch a ride on the fur (or sock/shoelaces) of an unsuspecting animal and hitch a ride to a new location.

In the race for global domination, filarees have also benefitted from the unsolicited help of many insects – perhaps most notably, ants. Ants will harvest filaree seed and bring it back to their little underground nests, effectively planting it (I have actually seen ants harvesting and hauling filaree seed!). And since filaree seed has been shown to be viable after 37 years of dormancy - that's not a bad way to invest in the future! It also doesn’t hurt that one robust plant can produce nearly 10,000 seeds in a single growing season.

Doin' the dirty work...

That's a hot mess of filaree seed!

       

From a physiology standpoint, research about explosive seed dispersal and hygroscopic coiling in plants provides invaluable insight into the mechanics of invasiveness for this abundant little herb. But all that science-y crap aside, this is just f***ing awesome!

Image and video credits:

http://www.troll.me/meme/war-cat

http://gifsoup.com/view/2686919/napoleon-dynamite-slap.html

https://conpm.wordpress.com/2009/04/19/erodium-cicutarium/

http://memecrunch.com/meme/M44F/if-you-want-peace-you-must-prepare-for-war

http://www.bio.utexas.edu/courses/bio406d/images/pics/ger/erodium_cicutarium.htm

https://thegardenimpressionists.wordpress.com/2011/10/26/pictures-speak-louder-than-words-fading-gracefully-and-last-pickings/

http://rsif.royalsocietypublishing.org/content/9/69/640.figures-only

http://jeb.biologists.org/content/suppl/2011/01/22/214.4.521.DC1

http://arizonabeetlesbugsbirdsandmore.blogspot.com/2012/04/backyard-ant-hills.html

http://knowyourmeme.com/memes/mind-blown

References:

Abraham, Y., C. Tamburu, E. Klein, J. W.C. Dunlop, P. Fratzl, U. Raviv, and R. Elbaum. 2012. Tilted cellulose arrangement as a novel mechanism for hygroscopic coiling in the stork’s bill awn. Journal of the Royal Society Interface 9:640-647.

Evangelista, D., S. Hotton, and J. Dumais. The mechanics of explosive dispersal and self-burial in the seeds of the filaree, Erodium cicutarium (Geraniaceae). The Journal of Experimental Biology 214:521-529.

Francis, A., S.J. Darbyshire, A. Legere, and M. Simard. 2012.The Biology of Canadian Weeds. 151. Erodium cicutarium (L.) L’Her. Ex Aiton. Canadian Journal of Plant Science 92:1359-1380.