A Darkling Path through the Ferny Ferns

Be there dragons here?

It's November and The Monthly Fern series is winding down. Looking back, I realized that most of the ferns I chose are distinctive—they're aquatic or have dimorphic leaves or are primitive lycophytes or grow large enough to inveil a romantic tryst! So this month's post will feature the ferny ferns (my term)—the ones we immediately recognize as ferns. However, figuring out which specific kind isn't guaranteed. If only ferns had flowers—so showy and diverse! Instead we must rely on leaves (1).

As the days shorten it would seem that writing descriptions for our Guide to South Dakota Plants would be appealing, especially given my current subjects—ferns and their relatives. But they can be difficult, and at times inscrutable. Of course they aren't the ones to blame. We are—specifically we botanists who seek order in their labyrinthine world.

I try to make my plant descriptions user-friendly, as our intended audience is broad—professionals, academics, students, enthusiasts, and eager novices (2). Being online makes this much easier. There will be many photos so I can shorten the text and minimize technical terms. Even so, there remain features that must be explained, for example the lovely lacy leaves of the ferny ferns.

The much-divided leaves of ferny ferns are the basis for "fernlike"—for example, "Western Yarrow leaves are fernlike" (SAplants).

Fern descriptions typically start with the plant—height, form (erect, spreading, sprawling), behavior (colony-forming, clumped), and other fairly straight-forward things. Leaves are next. Position (basal, on the stem), color, dimensions, and overall shape are easy to describe. But then ... we're faced with the dreaded degree of dissection. How many times is the leaf divided? Are there true segments? Are the segments themselves divided and are these divided as well? Here the guides I've been using as examples diverge, perhaps out of confusion. Suddenly the way forward becomes unclear; the path darkens considerably.

Entering the darkling world of leaf division.

"Leaf Division" from Fern Structure (USDA Forest Service).

In my web wanderings, I found a figure showing degrees of leaf division (above). It seems clear, though one needs to know that "pinnate" means divided and "-fid" means "nearly". For example, "pinnatifid" means nearly once-divided—division doesn't quite reach the midrib of the leaf as it does in "pinnate".

I intend to use this figure, perhaps as a pop-up, but will replace "pinnate" with "division" thereby eliminating the need for translation. "fid" situations will be accommodated with "nearly", for example "nearly twice-divided".

My version—actually a common approach, not my invention. 

Declaration of degree of division is followed by description of the ultimate segments—their shape, size, hairiness, margins, and such. This can provide much-welcomed help with identification. 

Ready for a test? Using the photos below, describe leaf division in Male Fern, Dryopteris filix-mas, and characterize the ultimate segments.

Male Fern's clumped ascending leaves can be more than a meter long. Аимаина хикари

Once-, nearly twice-, or twice-divided? Note the toothed (but not spiny) margins of the ultimate segments (click on image to view). Nick Turland

The sources I use all say that leaves of Male Fern are nearly twice-divided (pinnate-pinnatifid). But you needn't feel bad if you chose a different answer—you are correct. Male Fern leaves are usually once-divided at the tip, often twice-divided near the base, and nearly twice-divided in between. But adjacent segments can differ as the photo shows. Some are true segments, with division reaching all the way to the midrib. Others don't quite make it.

With no obvious path through this shadowy world, let's change the subject.

It's not uncommon for fern identification to be difficult, as even experts acknowledge (e.g., Cobb et al. 2005):

"Many ferns are distinguished by the finer details of the blade and how it is divided, and descriptions of fern blades can seem difficult and frustrating to beginners" (italics mine; I too get frustrated, and take offense at being labeled a beginner).

This is where a truly user-friendly guide can help, with lookalikes and tips for identification.

Be discriminating in your choice of guides.

In South Dakota we have an especially fine (= difficult) example of lookalikes—Fragile Fern vs. Oregon Cliff Fern. They grow on the same types of sites and look oh-so-similar. Both have nearly twice-divided leaves (often twice-divided at the base) and their ultimate segments have rounded tips and toothed margins.

Fragile Fern, Cystopteris fragilis (MWI).

Oregon Cliff Fern, Woodsia oregana (MWI).

Several small but distinctive features can help with identification (10x magnification recommended). Ultimate segments of Fragile Fern are not glandular and usually hairless, and the margins are irregularly toothed. In contrast, Oregon Cliff Fern segments are glandular hairy (more so on the underside), and the margins are regularly toothed.

Fragile Fern, with irregularly toothed segments (MWI).

In Oregon Cliff Fern, segments are regularly toothed (MWI).

Those familiar with these ferns in the wild have another tip, and it's something that's easier to see. Our Cliff Ferns (Woodsia species) often have persistent dead leaf stalks. This isn't the case for Fragile Fern.

It's not unusual for a mature Cliff Fern to have more dead stalks than leaves (Andre Zharkikh).

You can relax now. No more tests. We're very close to the end, with reassuring light visible ahead. And if you found leaf division tedious and difficult, think how I must feel after attempting to explain it! Sometimes I have to remind myself that I love plants.

Notes

(1) Replacing fern terminology—frond, stipe, pinnae, e.g.—with the more familiar terms used for angiosperms—leaf, leaf stalk, leaflet—has become fairly common (for example, Flora of North America). Others adhere to tradition, explaining terms in a glossary or introduction (for example, Cobb et al. 2005).

(2) I'm not enough of an expert to write descriptions of South Dakota plants myself. Instead I rely on the knowledge of others, both in printed manuals and online. The majority of photos also are by others, available online through Creative Commons licenses.

(3) Some readers may be thinking, "Just find fertile leaves with sori!" (spore clusters). After all, we've been told repeatedly that sori are distinctive. But those of Fragile Fern and Oregon Cliff Fern are hard to distinguish at maturity. Fragile Fern does have distinctive pocket-like indusia, but only when young (see photo of leaf segments in post).

Sources

All fern art created with NightCafe AI Art Generator.

Cobb, B, et al. 2005. Peterson Field Guide to Ferns, 2nd Ed. Northeastern and Central North America. Provides excellent lookalike information and tips.

Minnesota Wildflowers, a guide to the flora of Minnesota. This was the first online guide I found, and remains the most user-friendly of those I've seen (there aren't all that many, online guides being relatively new). Fortunately South Dakota and Minnesota share many plant species, and this website will be our main source of photos.

USDA Forest Service. Ferns. Highly recommended.

The Monthly Fern—More Quirks of Quillworts

Jon Keeley with several of his beloved quillworts (date unknown).

Once again The Monthly Fern series is featuring the Prairie Quillwort and its relatives—genus Isoetes. One post was not enough for these fascinating plants! Not only are they the sole survivors of a plant group that dominated 300 million years ago (see last month's post), they use CAM photosynthesis (1) ... that's astonishing! In fact it's so unexpected that when Jon Keeley announced it 40+ years ago, he was written off as ignorant (Keeley 2014).

Here's the conundrum. CAM photosynthesis is thought to have evolved in flowering plants (angiosperms) in hot arid environments. Many succulents, including most cacti, are CAM plants. But quillworts are primitive spore-producing lycophytes predating flowering plants by c. 200 million years. And almost all are aquatic.

Isoetes and other lycophytes split from ferns and seed plants long ago (source; black, red labels added).

Lycophyte diversity by Kingfiser (click link for full names and more info).

When I was an undergraduate long ago, only one type of photosynthesis was known (or so we were taught). As a grad student a decade later, I learned there were three: C3 is the common type; C4 and CAM are restricted to certain groups and situations (2). Since then I've largely ignored photosynthesis. But when I read that quillworts are CAM plants, I was intrigued! It was time to learn more. (Information here is from Khan Academy's Biology Unit 8, Photosynthesis unless noted otherwise.)

Photosynthesis: 1st stage powered by sunlight; 2nd makes food & oxygen for us to consume.

Photosynthesis is complicated and very chemical, but the basic process is simple. There are two stages. In the first, energy from sunlight is captured and converted to chemical energy. In the second, this chemical energy is used to convert carbon dioxide and water into glucose and similar carbon-based compounds, releasing oxygen in the process.

These are the benefits we reap. We consume carbon-based compounds for energy and to build proteins, DNA, muscles and more. And we breathe oxygen. If photosynthesis were to stop, we would die—either starve or suffocate.

As wonderful as photosynthesis is, there's room for improvement. The widespread C3 type, used by 85% of plants, is surprisingly inefficient. Carbon dioxide is captured and a sugar molecule created only about 65–80% of the time. The problem lies with an important but indiscriminate enzyme—rubisco—which will happily bind oxygen instead of carbon dioxide if given the chance (more here). 

Rubisco is the "molecular equivalent of a good friend with a bad habit" (KA, modified slightly).

This inefficiency is significantly less in C4 and CAM photosynthesis. But there's another problem and it's a big one—water loss. Plants take in carbon dioxide from air via stomata (pores) on leaf surfaces. But water vapor is lost at the same time, especially on hot dry days. Many plants close their stomata at night to prevent water loss, and when it's hot, some close stomata during the day as well. But then there's no source of carbon.

This is where CAM plants excel. They open their stomata at night and collect carbon dioxide, storing it for use the next day when the sun is shining. That way they can photosynthesize without opening their stomata and losing water. So clever!!

CAM photosynthesis requires extra energy compared to the common C3 type, but apparently it's worth the cost. CAM is used by at least 16,000 species, c. 7% of all plants. Most are desert plants, including at least 99% of the 1700 species of cacti (source). And then there are the quillworts, nearly all of which are aquatic at least part of their lives. Why would they bother with energy-expensive CAM?

Isoetes melanopoda, Prairie Quillwort, uses CAM even though it's aquatic (©2015 Robbin Moran).

Prairie Quillworts photosynthesizing by the light of day, with CO2 they gathered before dawn (Andrey Zharkikh).

Like terrestrial CAM plants, aquatic quillworts gather and store carbon dioxide at night but for a different reason. Terrestrial CAM plants have no access to CO2 during the day because their stomata are closed to prevent water loss. Quillworts have no risk of water loss, but for them daytime uptake of CO2 is difficult. It diffuses poorly in water to begin with, and most of the other plants in the pond are better at sucking it up for photosynthesis (4).

By the end of the day, the amount of CO2 in pond water is quite low. But as soon as night falls and photosynthesis stops, it quickly rises. "This must be when quillworts open their stomata to collect CO2" you may be thinking—as I did. But then a memory floated to the surface. Stomata don't work underwater! Aquatic quillworts have none, or non-functional ones at most.

From what I've read, there's still much to be learned about carbon dioxide uptake in Isoetes. However we do know that it varies with species and habitat. The few quillworts that are fully terrestrial—never submerged in water—have functional stomata and use C3 photosynthesis. They never use CAM, nor can they be converted to CAM even by keeping them underwater for a long time.

Isoetes histrix, Land Quillwort, is terrestrial (but often reported as aquatic). Late season photo by Sam Thomas; added insert by Peter de Lange.

Those quillworts that live part of their lives submerged, for example in vernal pools, are impressively versatile. They utilize CAM until water is low enough to expose their leaf tips to air. Then the stomata start to become functional and C3 photosynthesis begins to take over, progressing down each leaf cell by cell keeping just above the water! (Keeley 2014)

Isoetes howellii in dried vernal pool. It was in Howell's Quillwort that Jon Keeley stumbled upon CAM photosynthesis. © 2004 Carol W. Witham.

The many quillworts that are entirely aquatic are more puzzling. They have no stomata and their leaves are covered with a waxy cuticle. And yet they thrive, especially where other plants can't.

Aquatic Isoetes lacustris, the Lake Quillwort (Alina Ambrosova).

Isoetes lacustris in its favorite environment—lake bottom with sparse vegetation (5). (Alina Ambrosova) 

Aquatic quillworts seem to be more common in oligotrophic waters, where nutrients are scarce and there's little competing vegetation. So how do they survive if other plants can't? Probably with their unusual roots (6).

These roots have a large central air cavity that accumulates carbon dioxide gathered from sediments. Next to the cavity is bundle of vascular tissue that delivers it to the plant above. Furthermore, being CAM plants they collect CO2 at night as well as during the day, thereby doubling their harvest. Sometimes they truly flourish, covering the lake bottom in a dense green underwater carpet! (Moran 2004)

And with that, I will close. As you may suspect, this was one of my more challenging posts. Just when I had everything figured out, another puzzle would present itself. But I'm not complaining. In fact that's what I enjoy most about getting to know plants—pondering and unraveling their many little mysteries. And I know that the next time I meet up with a quillwort, it will be far richer experience.

So primitive, so simple in form, and yet so alluring (Isoetes englemannii, Nathan Aaron).

Notes

(1) C2 carbon concentration is sometimes considered a type of photosyntheses.

(2) CAM refers to crassulacean acid metabolism. To be clear, there is no "crassulacean acid"; the name refers to acid metabolism in the family Crassulaceae, where CAM was discovered (source).

(3) The widespread occurrence of CAM likely is due to repeated convergent evolution. After sequencing the pineapple genome, Ming et al. (2015) concluded that CAM arose from relatively simple reconfiguration of C3 pathways. See also Wickell et al. 2021.

(4) Many aquatic plants collect CO2 via bicarbonate; it appears that quillworts are unable to do this (Keeley 2014).

(5) Is that an alga on the leaves of Isoetes lacustris? If so, it might affect light capture but not CO2 uptake, which is done by the roots.

(6) Isoetes lacustris roots look very much like the fossilized roots of Lepidodendron trees, its ancient relatives.

Sources (in addition to links in post)

Keeley, JE. 1981. Diurnal acid metabolism in vernal pool Isoetes. Madroño 28:167-171. BHL

Keeley, JE. 1998. CAM Photosynthesis in submerged aquatic plants. The Botanical Review 64:122–158. PDF.

Keeley, JE. 2014. Aquatic CAM photosynthesis: A brief history of its discovery. Aquatic Botany 118: 38–44. http://dx.doi.org/10.1016/j.aquabot.2014.05.010

Lane, N. 2010. Life Ascending: The Ten Great Inventions of Evolution. WW Norton & Co.

Moran, Robbin. 2004. "Some Quirks of Quillworts" in A Natural History of Ferns. Timber Press.

Wickell, D, et al. 2021. Underwater CAM photosynthesis elucidated by Isoetes genome. Nat Commun. 12:6348 (open access).