Holy Hoppin' Horsetail Spores!

Equisetum hyemale is an able colonizer in spite of its lazy sporangia. Nevada roadcut, Matt Lavin photo.

Do you know the horsetails, also known as scouring rushes, genus Equisetum? They are curious plants, with slender hollow jointed green stems and no leaves (or so it appears). They're usually associated with water, but some make their way into human habitats—yards, pastures, and roadcuts for example. A small patch grows in my yard, next to the curb and gutter.

Equisetum's simple beauty. Unbranched species are often called scouring rushes. Andre Zharkikh photo.

Equisetum was once a member of the fern allies, along with moonworts, club mosses, spike mosses, and several other curiosities. Together with ferns, they sat between mosses and seed plants on the evolutionary ladder, having vascular tissue but no seeds. But because these plants looked very different from ferns and were poorly understood, they were thrown into a single catch-all group, even though they were diverse in appearance and structure.

Progress in evolution, left to right. The moss has no vascular tissue, so stays near the ground (source of water). The fern allies, fern, and flower are vascular plants, but only the flower is a seed plant.

Several decades ago, new knowledge did away with the fern allies group. Some members now reside in their own group, while others, including Equisetum, were combined with ferns. The expanded fern group was subdivided to accommodate the distinctive new members. The common familiar ferns of yore are now called true ferns for lack of a better name (leptosporangiates is the scientific name).

Though horsetails are technically ferns, their leaves differ radically from those of true ferns. In fact, at first glance it appears there are no leaves. But there are—just highly modified. Whorls of leaves occur at each node (not to be confused with branches in branched species). They are fused into a sheath that looks very much like the stem. The tips remain separate, forming a ring of "teeth" at the top of the sheath (deciduous in some species).

Tan sheaths are fused leaves, topped with a ring of black leaf tips (teeth). Matt Lavin photo.

Field horsetail, E. arvense, is a branched species. In the absence of green leaves, photosynthesis occurs in the stems and branches. Andre Zharkikh photo.

Another way in which horsetails differ from true ferns is in spore dispersal. They use a trick unique among spore-producing plants. Like true ferns, horsetails produce spores as fine as dust, in tiny structures called sporangia. But their sporangia are not terribly clever. Whereas those of true ferns are actual catapults that launch spores, sporangia of horsetails simply split open, dropping their spores on the ground.

In Equisetum, spore-producing sporangia reside in cones at tips of fertile stems. In field horsetail, fertile stems are flesh-colored. Green branched sterile stems emerge later.

For effective dispersal, horsetails rely on the spores themselves. Each one is wrapped in four ribbon-like appendages called elaters. Sensitive to humidity, they uncurl and curl back up with drying and wetting. Until recently, their exact function was unknown. It was thought that elaters probably acted like wings, helping spores fly with the wind.

Uncurling elaters of a horsetail spore. Source.

Then Marmottant and colleagues (2013) followed horsetail spores with a high-speed camera. They discovered that elaters function not as wings but as legs. Elaters allow spores to walk, and even better, to jump high enough to catch the wind!

Spores "walk" by extending their elaters with drying, and then shifting a little when humidity increases and the elaters curl back up. This is more like a random meander than a walk (image below), but it can get a spore out of tight situation, like being stuck to something.

If for some reason elaters can't gradually uncurl as they dry, elastic energy builds up until the stress is too great. Then suddenly the elaters uncurl, launching the spore. It may jump a full centimeter off the ground! This is a large distance compared to its size, and enough to catch a ride on windy days.

Spores can hop repeatedly because hopping doesn't damage the elaters. The authors of the study speculated that because jumps occur with drying, they are a way to escape from dry locations, hopefully to places with more moisture. The authors also "believe that this study will inspire new biomimetic classes of self-propelled objects ... ". Will groceries one day hop to our doorstep?

The image above shows a field horsetail spore in action. Top left—elaters partly uncurled with drying. Bottom left—path of spore "walking" in response to repeated changes in humidity; average step is 31 µm. Right—hopping horsetail spore in its first 3 milliseconds of travel after taking off at a speed of 0.35 m/sec. Modified from Marmottant et al. 2013.

If a spore lands in a suitable spot, it will germinate not into a horsetail like its parent, but a prothallus, the gametophyte or sexual plant that is part of the life cycle of all ferns. For a simplified version of the full story, see my previous post "Fern Seeds?"

Equisetum gametophyte; those of true ferns are typically heart-shaped or bilobed. Source.

Sources

Llorens, C, et al. 2015. The fern cavitation catapult: mechanism and design principles. J. R. Soc. Interface 13: 20150930. https://royalsocietypublishing.org/doi/10.1098/rsif.2015.0930

Marmottant P, Ponomarenko A, Bienaime ́ D. 2013 The walk and jump of Equisetum spores. Proc R Soc B 280: 20131465. http://dx.doi.org/10.1098/rspb.2013.1465

Moran, Robbin. 2004. A Horsetail's Tale? in A Natural History of Ferns. Timber Press.

Fern Seeds?

Woodsia (left) and Polystichum; from "A popular history of the British ferns" 1862, BHL.

Today we start with a quiz with one question:

TRUE or FALSE? Spores are the seeds of ferns. Just as a pea gives rise to a seedling, which grows into a full-sized pea plant, a spore gives rise to a baby fern, which grows into a full-sized fern like its parents.

And the answer is ...

Prothallus of Aspidium (wood fern; probably today's Thelypteris). Source.

... FALSE! A spore germinates to produce a prothallus, which can reach full size (ca. 1–2 cm across) in a few months.

Maybe some readers are surprised. Probably some knew the correct answer, or answered correctly because one choice seemed too obvious. Or maybe you were as I was last month—scratching my head trying to remember the fern life cycle, "the bugbear of many introductory botany students" (Moran 2004). This is unfortunate. Off-putting diagrams and terminology shouldn't keep us from the fascinating story of fern sex!

In an earlier post, I explained that I'm part of a group of botanists revising Vascular Plants of South Dakota by Theodore Van Bruggen. Currently I'm immersed in the world pteridophytes—ferns and their allies—which makes me a pteridologist, or at least an aspiring one.

In the fern section of the University library, I found A Natural History of Ferns by Robbin Moran of the New York Botanical Garden. His combination of science and stories has made my fernventures much more enjoyable. For example, the fern life cycle now makes sense. A light went on when I found a good starting point—the fact that fern spores, unlike seeds, do NOT produce miniature versions of their parents when they germinate.

Maybe you remember, maybe vaguely, that a typical fern has two life stages ... two independent free-living plants. The familiar one is the leafy fern plant, which produces spores. This makes it a sporophyte. The spores develop in tiny structures called sporangia, which form clusters on the underside of fern leaves.

Clusters of sporangia lined up on the underside of a fern leaf. Each sporangium is filled with spores. There may be several million spores in this view. Source.

Sporangia are much more exciting than their name would suggest. They don't just open, they don't even split suddenly. They cock themselves and shoot spores at speeds reaching 10 m/sec! (Llorens et al. 2015). Sporangia are catapults!!

The diagram below shows a sporangium catapult in action. Note the row of blue water-filled cells (a). When the outside surface of this row dries, it curves backward, opening the sporangium and cocking the catapult (b). This builds up elastic pressure until the row collapses suddenly, in just 30 µsec or so, sending the spores flying (c).

Modified from Llorens et al. 2015.

Fern spores are as fine as dust and can travel far. One lucky enough to land with its brethren in just the right place will germinate to produce not another familiar fern plant, but rather a stemless, rootless, leafless, tiny plant called a prothallus. What's the point? Sexual reproduction! The prothallus is a gametophyte, a producer of gametes (like pollen and ovules, sperm and eggs). The gametophyte is where fern sex happens.

Fern gametophytes are often heart-shaped or ~bilobed. Richard Droker photo.

A fern gametophyte is a simple structure, like a tiny piece of green lettuce when viewed from above. But on the underside are hairlike rhizoids that anchor it in place, and the very important antheridia and archegonia, which produce sperm and eggs respectively.

In the presence of water, sperm are released and swim off in search of sex. With luck, a sperm will reach an archegonium, either on the same gametophyte or often on an adjacent one. There it winds its way down through the cells of the "neck" and fertilizes the egg cell at the base. The result is a zygote, which produces the first leaves of the sporophyte as the gametophyte disintegrates. It continues to grow to become a familiar spore-producing fern. And so the cycle continues.

Young fern leaves growing from zygotes on disintegrating gametophytes. Richard Droker photo.

There is no seed anywhere in the life of a fern! Modified from source.

It took a long time for botanists to agree that ferns do not produce seeds. Even the great botanist Carl Linnaeus was sure fern seeds existed, though he wasn't sure where. "[I] must confess my ignorance whether what I see [today's spores] is seed, or dust of the anthers [pollen]" he wrote in 1737. By 1751, he had concluded the dust was indeed the miniscule seeds of ferns.

It wasn't until the mid 1800s that fern seeds finally vanished, as did their power. For there was a time when humans used fern seeds to great advantage. "We have the receipt of fern-seed, we walk invisible" cried one of Falstaff's thieving henchmen. Robbin Moran's book begins with this Shakespearean reference to fern seeds. But no spoilers here—you will have to read it yourself.

For more about the lives of ferns ...

American Fern Society. "About Ferns"

Brooklyn Botanic Garden. "How to Grow Ferns from Spores" 

Llorens, C, et al. 2015. The fern cavitation catapult: mechanism and design principles. J. R. Soc. Interface 13: 20150930. https://royalsocietypublishing.org/doi/10.1098/rsif.2015.0930

Moran, Robbin. 2004. A Natural History of Ferns. Timber Press.

USDA Forest Service. "Fern Reproduction"

Tree-following in the Footsteps of Wyoming Botanists

Balsam poplar in Montana in August. Photo by Matt Lavin who writes: "Balsam popular is the most common poplar in montane riparian settings in western Montana."

Last week we had snow and bitter cold (-16ºF in town one morning). This weekend the snow is melting fast, turning roads and trails to slush and mud. So I decided not to visit my trees, an aspen and a balsam poplar, which I'm sure are as dormant as I feel these days. Oh spring, where art thou?!

Instead, I checked online to see where balsam poplar grows in our area. Although it's common nearby to the south in the mountains of Colorado, it occurs only sporadically in the mountains of southeast Wyoming.

SEINet search results for Populus balsamifera, displayed in Google Maps.

An online search of the Rocky Mountain Herbarium at the University of Wyoming produced four specimens from the area where my tree grows (see map above). All were collected by Cedric L. "Ted" Porter, including two with his wife Marjorie. Ted and Marjorie arrived in Laramie in 1929, traveling from Ohio in a Model T Ford. Ted had been hired as Botany Instructor and swim coach at the University of Wyoming. In 1937 he was promoted to Assistant Curator of the Rocky Mountain Herbarium, and then Curator when the great Aven Nelson, who started the herbarium in 1899, retired in 1943.

Porter served as Curator until 1968. During that time, the number of specimens grew by almost 50%, in part through Porter's collecting and trading of duplicates with other herbaria. His careful organized approach to curation made the Rocky Mountain Herbarium "probably the best organised, curated, and housed medium-sized herbarium in the nation" (Hartman & Nelson 2000. Cedric Lambert Porter (1905-2000) Taxon 49:577-580).

In 1962, Ted and Marjorie collected balsam poplar "at the Tie City Campground" in the Laramie Range. Here we enter the foggy slippery frustrating world of history. The Porters collected balsam poplar along a stream, but Tie City Campground is not on a stream, at least not today. Instead it's on a broad ridge crest, at a site some of us call Upper Tie City. Probably today's Pole Creek Campground was where the Porters collected. A stream runs along one side, and balsam poplars grow there, including the one I'm following.

Pole Creek Campground area in early January ... much warmer then!

It appears Ted and Marjorie were particularly interested in the balsam poplars because they made two collecting trips. The first was on June 1, when the trees were in late flower/early fruit. Below are images of their very nice specimen, showing young fruit with lobed stigmas. Like most poplars, balsam poplars are dioecious. This specimen is a female tree.

The Porters returned to Tie City Campground on July 26 and collected more material, this time to show the distinctive bicolored leaves (pale undersides).

Closeup of label; note habitat: "along stream."

It has been wonderful to get to know the Porters better, especially after hearing their names for 40+ years! And now when I visit I will be following ghosts as well as trees—something I enjoy very much.

This is my contribution to the gathering of tree followers kindly hosted by The Squirrelbasket. Want to give it a try? More info here.